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DISPERSAL IN RODENTS:
A RESIDENT FITNESS HYPOTHESIS
SPECIAL PUBLICATIONS
This series, published by the American Society of Mammalogists, has been established
for papers of monographic scope concerned with some aspect of the biology of mam-
mals.
Correspondence concerning manuscripts to be submitted for publication in the series
should be addressed to the Editor for Special Publications, Jerry R. Choate (address
below). :
Copies of Special Publications of the Society may be ordered from the Secretary-
Treasurer, H. Duane Smith, 501 Widtsoe Bldg., Dept. Zoology, Brigham Young Uni-
versity, Provo, UT 84602.
COMMITTEE ON SPECIAL PUBLICATIONS
Jerry R. CHoate, Editor
Museum of the High Plains
Fort Hays State University
Hays, KS 67601
Don E. Witson, Managing Editor
Bird and Mammal Laboratory
National Museum of Natural History
Washington, DC 20560
EDITORS FOR SPECIAL PUBLICATION NO. 9
ELMER C. Birney, Editor
Bell Museum of Natural History
University of Minnesota
Minneapolis, MN 55455
CARLETON J. PHILLIPS, Managing Editor
Department of Biology
Hofstra University
Hempstead, NY 11550
Dispersal in Rodents:
A Resident Fitness
Hypothesis
PAUL K. ANDERSON
Department of Biological Sciences
University of Calgary
SPECIAL PUBLICATION NO. 9
THE AMERICAN SOCIETY OF MAMMALOGISTS
PUBLISHED 30 Marcu 1989
hz
JUL 65 1999
HARVARD
UNIVERSITY
Library of Congress Catalog Card No. 88-072153
© 1989 by The American Society of Mammalogists
ISBN No. 0-935868-40-2
Foreword
Rodent populations are relatively accessible for study and experimental manipulation, and
behavior of at least some diurnal species is easily observed. As a result, rodents have attracted
the attention of students of behavior and population biology and a massive literature has been
generated, so much so that the accumulation of observations threatens to inhibit synthesis and
the evolution of cohesive theory. Demographically inclined ecologists, in particular, have found
rodents of interest and there has been a major focus on the role of dispersal (narrowly defined
as emigration) in population regulation. I believe, as suggested by Jannett (1980), that this
demographic emphasis has led to biases and misinterpretations of the available data, and has
led the study of dispersal up a blind alley or, as others have put it, to a theoretical impasse
(Gaines and McClenaghan, 1980).
If there is indeed an impasse, the blame cannot be laid entirely on the demographers. I propose
two other villains, the first of which is the imprecise use of language. Aldous Huxley is said to
have declared that language perverts thought. Huxley’s point is most appropriate: vague and
misleading usages have greatly hindered our thinking about the subject of dispersal. I have
focused on semantic difficulties in Chapter I, hoping to lay an unambiguous foundation for what
follows. The other source of difficulty, as I see it, is the too-facile assumption that because animals
emigrate, there must have been direct selection for emigratory tendency. I refer to this assumption
that the evolution of dispersal is founded on benefit to emigrants as “the emigrant fitness
hypothesis.” Chapter II deals at length with the question of whether this hypothesis is adequately
supported.
In Chapter III, I advance an alternative hypothesis: the results of my attempt to approach the
topic of dispersal from the perspectives of behavioral ecology and evolutionary theory. The
emphasis is place on such concepts as inclusive fitness and parent-offspring conflict, and a
consideration of parental strategies that extends beyond the conventional view of parental in-
vestment. I present ideas as to dispersal mechanisms on the basis of these parental strategies and
their evolution, and suggest deductions that may shed new light on some demographic problems.
Chapter IV deals with the alternative hypothesis in the light of a selective review of the
literature. This has been a daunting task, and one that could be continued almost indefinitely.
I have tried to be reasonably comprehensive, because that is what testing the hypothesis in this
preliminary way requires, but it was neither possible, nor desirable, to be exhaustive. I hope the
reader will find the treatment reasonably unbiased and adequate without it becoming tiresome.
In Chapter V, I have ventured a series of predictions and possible tests of the new hypothesis.
If the predictions are testable, and at least some suggested tests can be implemented, our
understanding will be advanced and this book will have served its purpose, regardless of whether
my alternative theory is supported or rejected.
Chapter VI is a brief concluding statement. In it I have tried to draw attention to the elements
and implications that I regard as the core of the Resident Fitness view of rodent dispersal.
Like all ideas, those I have expressed could never have evolved without the work of numerous
investigators, both those whose work I have cited and others not so mentioned. I am equally
indebted to mammaologists whose work I may have criticized, or whose conclusions I have
disagreed with, as well as those whose interpretations fit neatly into my perspective.
For critical reading of parts or all of the evolving drafts I am grateful to Kenneth Armitage,
Mark Bekoff, Andrew Blaustein, Elmer Birney, John Eisenberg, Michael Gaines, Lowell Getz,
Michael Johnson, Robert May, Douglas Morris, Robert Rose, Peter Waser, and two anonymous
reviewers. Thankfully, not one agreed with all I have proposed. Their criticism, their willingness
to give thoughtful consideration to unconventional ideas, and their suggestions are greatly ap-
preciated.
Very special thanks go to Elmer C. Birney and Carleton J. Phillips for their editorship, and
to my wife, Donna Anderson, whose proofreading and checking of citations has been invaluable.
Last, but not least, I would like to express my gratitude to The American Society of Mammalogists
and its Editorial Committee for the opportunity to present my ideas in the form of a Special
Publication.
I dedicate this book to all those small furry travelers whose paths have crossed mine, so often
to their distress. May their alleles prosper.
vi
CONTENTS
I
Starting Points
ALTO UCtIO Mien ny Seat eC wren Ew OU yal ame MM hic os ats alld Hee aca hee
nhemMenninoloryaonmDispersalamps. faa file Ac Anti nts Ae 2h es Soeede. chs ttm aud o eee
EnacticalwAspectscor Categorization) # yy qr aan e en. . Sola lod Aes. 6 kOe ae
Baseliney@Olsenvali@istew, mrEni i. ae we Meenas |i cette! nevoden sca 4 lt aye cluate oes
Riess MVM natsam anton MOM! 4-99 sh se etter. fi Sh 4 Ph ee
II
The Emigrant Fitness Hypothesis
ATEN UCU O Na OME eT SN Rese oe ey Sis Che. neeecas n=, Pe aR a POLI ee tha. ay
PRSSMIIN tL OUSHO Hate RES Ll ona hee es itd ae Mtado ms § Ramla eal on cc ee Se
alstialbilitygOrtherbulom er. «soon «eee Sec ets 8) MENG Ao, ee Semen Ete, oe
Increased Fitness Through Emigration: Survival of Emigrants......................
Increased Fitness Through Emigration: Avoiding Competition .....................
Increased Fitness Through Emigration: Opportunity for Breeding
Increased Fitness Through Emigration: Immigration and Breeding .................
Increased Fitness Through Emigration: Establishment in Better Habitat ............
Increased Fitness Through Emigration: Emigrant Advantage Through Heterotic Mating
Increased Fitness Through Emigration: Avoidance of Inbreeding Depression ........ .
Increased Fitness Through Emigration: Avoidance of Population Crashes ............
ihesKividence tor Emigration Brone-Genotypes;. 20...) 0).
REjech Onno mths Liubligner me menran ea tinet soe near 2, ik Loe Leben ade ante he
Ill
The Resident Fitness Hypothesis
WTAE OCU EL OTT Sey ewes Pe YOR a a Senne Bat teh i on ac Hae cone, le ati a nl I ty Be
Elabitatshleterogeneltyamrasn sre skied bile AMP a seedel tae 8 Seat Red Aen: fay a Real Foie ee ee
Strate siessormlWesiaent Rodents» ool are. G kee Ses MS oe ee ee ee
StratesiesstomhesicentsMalesnpy ie saeco tpi eh ets eh). Bae ghia ale ee yee oe
Implications of Strategies Postulated for Resident Males ...........................
StrategiesmorehesidentwHemaless m aher ities ye. wiser ere on ys Mae a eed Soke:
Implications of Strategies Postulated for Resident Females.........................
State gt esrrora@ fsprim cease tipi tasers ce Ta Nereis 5 hb ee Ut ge hie ie 8 ie yan yl es
Strategiestion VMale@fisprimgi efi & Seth ets eh rat ac ee ee: fk deeiy oeontr!
Implications of Strategies Postulated for Male Offspring
Strategiesiorsemale) @lts prin gare eps Aas 1 Ot: Bae ps Ac eee oneal:
Implications of Strategies Postulated for Female Offspring
Strategresplore. Lransientsecben ite, Men a rueste errs cede ee nets oD ead trodes ome webee es
Implications of Strategies Postulated for Transients
Summary
vil
© OWE
10
10
10
10
12
14
M7
19
20
21
25
26
27
29
31
31
30
36
37
38
39
4]
4]
42
43
43
44
44
Introduction
IV
Testing the Resident Fitness Hypothesis Against
Observations in the Literature
dihersite Menacitya ofslvesia ental Od erts aise rt sean treo
ihe Brevalence andslmpontancelof: ehilopatiy ee ae eee
Discrimination Among Relatives, Associates, and Transients .......................
CohesivenesssAmongakGneny ee ee ee Teo ab Byte th eget er ee ge a
MatingePreferencesrotaesidentsis.— 5 aetna. ee clea e e e e
HowAComuionsissinbreedingiate: . 6.0 ae a No nae con ae ee
Barniecrsitovnbreedinpmrmene oer! ako 5 bette ep Skye en ene eee
Malei@orpetitronston Copulations sey en ee ee ee
Residents Malembehavion lowaxcds@lsprinyenmee aren) ee ee
CompetitionsandyNgoression imphemalesRodents) 9400 45- 555500400 gee eee ae aoe
ResidentakiemaleaNcpotismmmant, cae tres se secs cette eau iied cl ol ty Arh nen ee
mhibitioniol immiugration by, Residents)... 95-45-45 ee ee
ihe: Stimmuliptor emigration: 0.0.1 20. wuss Sayan Sad d geage eo oe, Ge ee
Resident Behavior as a Cause of Emigration of Offspring ..........................
Resident Male Aggression and the Export of Offspring ............................
Resident Female Aggression and the Export of Offspring ..........................
ReEsponsesiol Youngatoyhesid ent Bressuies sae ry see es see aoe
Responses ol Male Offspringayn aAaan aves ity eee: «ey ee ee ee
Responses'on Female Oftspning.9: iy 4. faulrab sete. ee ee, eee ee
The Confinement Syndrome: Consequences of Lack of Egress......................
Summary ...
Demographicsbredictions;and)lestsin 14.4.9) se ee ee
Geneticyeredictionsrand:-Vests® © khan. Pee eh ete OOS UPN, Op 20 Re Nie aes oe
Summary ...
Ag Concluding; Statement ys ec. hyo. Nees easter ca Se ae
Hiten ate Giese. see Ades ao ahaaas, naG WER? ae ene y's he a a a
Indexae ee
vill
I
STARTING POINTS
Arguments have been advanced for the adaptiveness of dispersal in both stable (Comins et
al., 1980; Hamilton and May, 1977) and variable (Cohen, 1967; Levins, 1968) environments.
The latter will most often apply to rodents because extinction and recolonization are frequent
in the habitat patches occupied by small mammals (e.g., Myllymaki, 1977b; Pokki, 1981; Smith,
1980; Tomich, 1970). As a result most lineages ultimately persist only through the success of
their disseminules. Similarly, environmental stochasticism dictates that the perpetuation of an
allele, a gene combination, or a chromosomal arrangement requires the transfer of copies of
genetic information, or of individuals that then succeed in transmitting it, to new locations (Van
Valen, 1971).
Unlike the perpetuation of an allele or a population, the limited history of an individual can
proceed without dispersal. Nevertheless, individual fitness will rarely be unaffected by the choice
between philopatry and emigration, and although the individual's requirement for dispersal is
less, the cost to the individual may be greater. If an individual emigrates, the process consumes
part of a finite life span. Time spent moving may reduce the time available for reproduction,
and the movement itself entails risks that must be accepted in return for uncertain rewards.
Despite these costs and uncertainties individuals do disappear from their natal sites, transient
individuals can be identified, vacant sites are colonized, and individuals carrying new alleles do
sometimes become integrated into existing populations. What mechanisms are involved in the
emigration of individuals, their subsequent wanderings, and the eventual immigration of those
that succeed in reproducing in new locations? How might the genotypes underlying the behavioral
phenotypes influencing these processes be selected?
The Terminology of Dispersal
Discussion of dispersal suffers from ambiguous terminology. Vague and varying usages create
difficulties in communication, even an inability to understand what we ourselves are thinking
or saying. Although nature is not overly friendly to precise definitions, nor bound by them,
communication is dependent on precision and consistency. My objectives in the following para-
graphs are to establish an unambiguous set of definitions. First, I wish to emphasize that weanlings,
juveniles, subadults, adults, residents, emigrants, transients, and immigrants are classes of indi-
viduals with distinctly different status in terms of social interaction, demography, and repro-
ductive potential. Failing to recognize distinctions among processes, and among individuals of
different status in populations, can only garble our data and befuddle our thinking. Differing,
and often indeterminate, classifications of the stages of individual ontogeny can be baffling.
Therefore, the first set of terms has to do with ontogenetic stages that I regard as important in
the study of dispersal.
Weanling.—Weanlings are recently weaned individuals that are not yet approaching adult
size or sexual maturity and that limit their travels to exploration in the vicinity of the natal site.
Natal range.—Unless weanlings show the site attachment, homing tendency, and site-depen-
dent dominance that characterize occupancy of space by resident adults, the term “natal home
range’ (Bondrup-Nielsen, 1985) seems contradictory. “Natal range” seems a preferable and
adequate term by which to refer to the space defined by the initial travels of weanling and
juvenile individuals.
Bondrup-Nielsen’s (1985) point that space use goes through ontogenetic changes is important,
however, because the distinction between adult and non-adult site occupancy is often overlooked.
1
2 Rodent Dispersal
Failure to implement such a distinction makes such definitions of “dispersal” (=emigration) as
movements of individuals in which they leave their home range (e.g., Stenseth, 1983) inappro-
priate if the majority of emigrants have not previously exhibited the qualities which characterize
occupancy of home range in adults.
Juvenile.—The term juvenile has been variously applied. Commonly it refers to pre-pubertal
individuals. Following weaning, rodents may progress rapidly into and through puberty (e.g.,
young microtines born early in the breeding season) or delay puberty for many months (e.g.,
microtines born late in the breeding season). Although I visualize no clear demarcation between
weanling and juvenile stages, it seems best to use the term “juvenile” to refer to a post-weanling,
pre-pubertal phase of life history. Juveniles can attain adult size and establish site tenacity without
being sexually competent. In some seasonally breeding species, such juveniles can make up the
bulk of the population just prior to the initiation of a breeding season. I therefore define a juvenile
as a post-weanling, pre-pubertal individual.
Subadult.—I define a subadult as an individual in the process of sexual maturation. Subadults
are not treated in the same ways as weanlings or juveniles and can come under social pressure
as puberty proceeds. Although subadults are capable of producing viable gametes, they are
neither socially nor spatially established and are unlikely to breed. Puberty is often the period
when parent-offspring conflict peaks and the period when offspring cease to be recipients of
parental investment and come to be treated in the same way as other relatives. Although such
individuals might be repeatedly encountered in the natal range, one cannot assume that they
have developed the site attachment, or the associated psychological and social status, of residents.
Adult.—Most rodents are seasonal breeders and a fully grown individual might or might not
be sexually active. Traditionally, adulthood has been equated with sexual maturity. If this is to
be the sole criterion, an “adult” can be defined as an individual that is either sexually competent
or has been so. If there are good grounds for the position that socio-spatial status is as important
as sexual status, an adult is an individual that conforms to the sexual criteria above and is either
established in a spatio-social context (i.e., occupies a home range) or has been so in the past. I
use the term adult in this way because otherwise definitions of “dispersal” (=emigration) such
as “movements of individuals in which they leave their home range’ (Stenseth, 1983) are
inappropriate if the majority of emigrants have not previously been spatio-socially established.
Resident.—A resident individual can be defined as a juvenile, subadult, or adult that has
established a home range. In the past, tests for residency and non-residency often have not been
satisfactory. Empirically, residency usually has been identified by consistent presence within a
limited area. A better experimental criterion for residency is that a resident individual should
attempt to “home” when displaced. Karlsson (1984) demonstrated residency as a difference in
orientation in a laboratory apparatus. Overwintered and sexually active (adult), and overwintered
but not yet sexually active (juvenile), Clethrionomys oriented toward the homesite, whereas
young of the year did not. Because homeward orientation was displayed in spring, Karlsson’s
results indicated that juveniles had established their residency in winter.
The use of homing as a criterion by which to distinguish between residents and non-residents
should be explored further. Although home range should be a dynamic concept (Madison, 1985),
site tenacity and associated behaviors are a distinctive aspect of rodent ecology and must be
fully taken into account.
Emigrant.—Once weaned, an individual is physically capable of leaving the natal site. To
refer to any such one-way movement I will follow here a usage proposed in an earlier paper
dealing specifically with microtines (Anderson, 1980); the terminology is close to that of Moore
and Ali (1984). Emigration will refer specifically to departure of an individual from either its
natal range or the home range on which it had been established. An emigrant is an individual
in the process of departure. The important elements that define emigration are one-way move-
ment, extraction of the individual from any reproductive and social relationships in which it has
participated, and extraction of the genetic information it carries from the local gene pool. In
practical terms, extraction from the previous set of social contacts can be defined as movement
Starting Points 3
beyond the boundaries of the area of previous activity that are in excess of one home range
diameter. This criterion serves to distinguish between emigration and range shifts or changes of
home site that are not sufficient to remove an individual from former social relationships and
potential or actual mates. Beyond that limit there seems to be no reason why either distance or
directionality should be specified.
Lidicker (1975) proposed two categories of emigration, which he referred to as “pre-saturation
dispersal” and “saturation dispersal.” The former described emigrants that moved out of an area
before peak density was reached, the latter those that emigrated at or subsequent to a peak in
density. Lidicker predicted that individuals in the pre-saturation category would be healthy
individuals with a high potential for survival and reproduction, whereas those in the saturation
category would be physiologically inferior, with low potential for survival and reproduction. It
is not clear whether we should expect a bimodality or the extremes of a continuum, but Lidicker
visualized pre-saturation dispersers as having “a particular sensitivity to increasing density”
(Lidicker, 1975:106).
Although the pre-saturation/saturation dichotomy is attractive at first sight, I believe it should
be discarded. It seems to me that the evidence reviewed below shows that young are inherently
philopatric, and will be likely to maximize fitness by establishing at the natal site. Further, it is
a logical and semantic trap to accept the a priori assumption that emigration is density dependent.
I suggest emigration can be expected only when a potential emigrant perceives its physical and
social position untenable (i.e., its personal environment “oversaturated’’). As perceived by the
emigrating individual all emigration may be ‘‘saturation” emigration. Such individual perceptions
may have no relation to density as measured by a demographer.
[also find it difficult to see how Lidicker’s terminology can be made operational because (from
the population viewpoint) “saturation” can only be defined after the fact on the basis of whatever
peak density happened to precede a decline, or by assuming a fixed carrying capacity. The
alternative of defining “saturation” emigrants (or transients) on the basis of individual condition
is unsatisfactory because not all ill, old, injured, starved, or socially outcast individuals are likely
to be associated with peak density, and healthy individuals should be as quick to leave as unhealthy
ones if their habit is destroyed. Furthermore, in practice the locations from which most transients
departed are unknown and therefore the conditions from which they took leave cannot be
determined.
Stenseth (1983) proposed abandonment of Lidicker’s terminology on the ground that there
was no theoretical reason why “saturation dispersal’ should be an adaptive phenomenon. He
proposed the alternatives of “adaptive (or evolutionarily stable strategy) dispersal” and “non-
adaptive dispersal,” referring to the latter as characteristic of “surplus” individuals. The point
made by Stenseth would seem to be that movements are adaptively irrelevant unless emigrants
are successful in immigrating. Stenseth’s approach avoided some of the biases inherent in a
preoccupation with density, but not others. Like Lidicker’s terminology, Stenseth’s carries un-
justified implications. It is not clear to me whether the term “surplus” refers to the carrying
capacity of the habitat, or to the “needs” of the population. It is reasonable to suppose that
individuals may move in the face of habitat destruction, or that individuals on the verge of death
may lose site tenacity. Stenseth did not, however, directly address the question of whether
emigrants do gain fitness, nor did he consider the possibility that the emigration of individuals
that eventually die without reproducing might benefit former associates that did not emigrate.
Perhaps the most telling point with respect to these attempts to define classes of emigrants is
the absence of data. I have not found in the literature any case where the existence of two
significant and distinct classes of emigrant has been convincingly demonstrated. The important
point that Lidicker (1975) raised is the need to explain emigration when it appears that there
are adequate resources at or near the site from which an individual departs. The alternative
dispersal hypothesis proposed in Chapter III deals with this point, and seems to me to account
for the observations that originally led Lidicker to propose the pre-saturation/saturation di-
chotomy.
4 Rodent Dispersal
Transient.—Upon emigration from a natal range or an established home range, and losing
contact with mates or other familiar individuals, an emigrant becomes a transient until a site
attachment is established. I specifically distinguish this definition from that of Flowerdew (1978)
who defined a transient as “any individual which is emigrating or immigrating.” I regard
emigration and immigration as specific states different from transiency.
Settler.—Transient status ends when a new site attachment is established. An individual can
then be referred to as a settler. Settlement implies residency but it does not imply reproduction.
If a transient settles in unoccupied habitat it is not required to establish itself in a resident group
(i.e., to immigrate).
Immigrant.—I will use immigration to refer to the process of establishment of a settler in a
new spatial, social, and reproductive context. Demographically, immigration need not imply
breeding, but from an evolutionary point of view immigration implies production of fertile
offspring in the new situation. In a genetic sense an immigrant has completed dispersal when
such young reproduce.
Mihok et al. (1985a) used “recruitment” as a synonym for immigration. In an evolutionary
sense this is misleading because recruitment does not necessarily imply movement from the natal
site, whereas immigration implies origin elsewhere.
Dispersal.—Despite common usage to the contrary, I strongly believe that the term “dispersal”
should be used only in its full evolutionary sense. Throughout this volume dispersal implies
emigration followed by immigration. In other words it will be equivalent to “effective dispersal”
(Greenwood, 1980) or “transfer” (Moore and Ali, 1984). I suggest it is best applied with the
understanding that the offspring produced after immigration must be both fertile and repro-
ductively successful.
The use of “dispersal” as a synonym for emigration is confusing, unnecessary, and generally
misleading. Although this misuse of the term is unfortunately imbedded in the literature, I hope
it eventually can be discontinued. Emigration is distinct from dispersal in that unless emigration
is followed by immigration it is in most respects the evolutionary equivalent of death.
With the possible exception of some spermophiles, I question the need to distinguish between
“natal dispersal” and “breeding dispersal” (Greenwood, 1980, 1983) in rodents. Although specific
data are scanty, it is my impression that rodents generally disperse only once, or not at all. No
one has shown that resident individuals forced to emigrate at the start of a breeding season (e.g.,
Fairbairn, 1977a, 1978a) are subsequently successful breeders (i.e., immigrate) elsewhere. Ground
squirrel populations in which successfully breeding males move to new homesites at the ter-
mination of the breedifg season (e.g., Sherman, 1980) may be an exception, but there is little
evidence as to the success of such males in overwintering and breeding a second time. It is
noteworthy that males that have not bred do not emigrate, and generally breed in the subsequent
season. . ;
[also feel that the word “disperser, as commonly used in literature, should be avoided because
of its ambiguity and its implication of goal or purpose. “Emigrant” is a simple, precise, and
readily understood alternative that describes an individual departing from a natal site or home
range. Similarly, “transient” accurately defines a wandering individual. If the term “disperser”
has any justifiable use, it is merely as a catchall to include emigrants, transients, settlers, and
immigrants whose exact status is unknown. As such, it is primarily a way of expressing ignorance
about the actual status of individuals and has little scientific value.
The foregoing definitions apply to dispersal in terms of an individual. There seems to be no
alternative to using dispersal in one sense for individuals and in another for populations. Within
populations, dispersal, as defined above, influences the evolutionarily effective population size
and the spatial distribution of an individual’s genetic contribution to subsequent generations.
Panmixia, which defines a population in an evolutionary sense, is a result of continuity of dispersal.
Attenuation of dispersal defines population boundaries. Between populations dispersal determines
gene exchange and introduces new alleles and gene combinations. Where habitat has been vacant,
dispersal may lead to founding of new populations. Krohne et al. (1984) attempted to deal with
Starting Points 5
this problem by defining dispersal as movement within a demographic unit (in practice a trapping
grid) and emigration as movement out of a demographic unit. This definition of dispersal is
counter to common usage in both population genetics and island biogeography and although I
understand their objective I feel their suggestion is likely to be confusing and counterproductive.
“Intra-population” and “inter-population” dispersal might suffice, provided the boundaries of
the deme have actually been determined.
Brooks and Banks (1973), Jannett (1980), Myllymaki (1977a), Tast (1966), and others have
described shifts of homesite and home range that I feel do not qualify as dispersal. In the
individual sense of dispersal as described above, a range shift qualifies as dispersal only if the
individual establishes a new set of social contacts and a new set of potential and/or actual mates.
In a population sense, range shifts may imply dispersal only if they transfer genetic information
to another population.
I would like to deal here with another term proposed by Lidicker (1975). Individuals that
would otherwise emigrate may be prevented from doing so by physical or social barriers. When
physical barriers are imposed as part of an experimental regime, behavioral and physiological
abnormalities often result (Anderson, 1961; Calhoun, 1962b; Krebs et al., 1969). Lidicker proposed
the term “frustrated dispersal” for such situations. It is not clear whether the term applies to
the inability of individuals to emigrate, or to the consequences of that inability for individuals,
or for populations. Bondrup-Nielsen and Karlsson (1985) regarded Lidicker’s term as internally
contradictory because emigration has, by definition, not occurred. I concur, and in my view it
is preferable to discuss the separate phenomena of obstacles to emigration, their effects on
individuals, and the consequences for populations, without use of an ambiguous umbrella term.
The emigration sink.—In the context of the definition of dispersal used here, “dispersal sink”
(Lidicker, 1975) is self-contradictory. “Sink” can be used in two senses. In the individual sense
the term implies absorption or dissipation of individuals: a “graveyard” (Stenseth, 1983). Indi-
viduals moving into a space in which they eventually die without leaving descendents have
entered a sink. Individuals written off demographically and reproductively, have, by my defi-
nition, failed to disperse. I therefore prefer the term “emigration sink.”
Complications arise when the sink concept is used in the population sense. With respect to
the source population, the disappearance of emigrants acts as a “behavioral vent.” Relative to
that population it is of no immediate consequence whether the resulting transients enter a
graveyard, join another population, or found a new population.
The common ground between individual and population viewpoints is that emigration results
in the elimination of individuals. This does not, however, completely resolve the problem.
Although any space into which an individual moves that is beyond the limits of the family or
deme from which it emigrated serves as a “sink” from the point of view of the source population,
transients, settlers, and immigrants are, in varying degree, still part of the metapopulation (sensu
Wilson, 1973). To avoid this difficulty I will use “emigration sink” only in the individual sense.
Philopatry.—Im a spatial sense, a rodent is philopatric if it establishes residence at its natal
site, within the home range of a parent, or in contact with the home range of a parent. In a
reproductive and genetic sense it is philopatric if it makes a reproductive and genetic contribution
to the ongoing lineage or local population to which a parent belonged. This approach implies a
definition of natal philopatry somewhat broader than that of Waser and Jones (1983) in that
individuals establishing home ranges in contact with those of parents or other closely related
residents would be considered to be philopatric in a population sense even though as individuals
they have dispersed when they establish home ranges and centers of activity, and breed, at
locations more than one home range diameter away from the natal site as specified above.
From the population viewpoint we are forced to think of dispersal within the population as
the factor binding the population into a genetic unit, and dispersal beyond the population
perimeter as a process that removes genetic information from the gene pool (emigration in the
genetic sense) and introduces it to other gene pools (immigration in the genetic sense).
Territoriality and spacing behavior.—The term “spacing behavior” appears to be coming
6 Rodent Dispersal
into fashion. I have not found a reference in which a formal definition has been offered and my
impression is that it has become popular as a substitute for territoriality. The essential charac-
teristics of territoriality are a fixed area of activity, and acts by the resident that serve to evoke
escape or avoidance by some class of potential occupants, leading to the exclusion of the latter
(Brown and Orians, 1970). Gauthreaux (1978) suggested that territoriality implied space-related
dominance which gave priority of access to a resource. He noted that status as a territory holder
might involve individual recognition and might serve in reducing the costs of interaction. “Spacing
behavior” seems to imply a broader scope, including individual distance and avoidance of contact,
but not necessarily requiring site attachment.
Perhaps what makes “spacing behavior” attractive is that it avoids two difficulties that often
cause misunderstanding with respect to territoriality. One is that animals may behave in a
territorial fashion with only partial success. For example, Wolff (1985b) noted that, in microtines,
exclusive home ranges may decrease in size to a minimum as density increases. He believed that
at high density at least some degree of exclusivity is lost. The latter point seems open to question.
In any event it is not clear that animals would cease to behave in a territorial manner, even
though they have been unable to prevent overlap. The second difficulty has to do with the
provision that a class of conspecifics is excluded. Many authors regard overlap of home ranges
in one sex as evidence that animals of that sex are not territorial. This misses an important point.
If, for example, there is overlap among male home ranges in a Microtus population, the overlap
may be limited to less than a half dozen mutually familiar adult individuals; others (the class of
unfamiliar or, possibly, unrelated adult males) may be excluded. Because a class of conspecifics
is still being excluded, perhaps as a result of cooperative site-specific dominance, my view is that
the behavior of the residents is territorial, as is the social system. Where site-specific dominance
is evident, it may still be best to refer to behavior of residents that appears to have evolved as
a consequence of its exclusion of any class of conspecifics (defined by sex, age, familiarity, etc.)
as territorial behavior.
Parental investment and parental disbursement.—A semantic dilemma arises in Chapter III
in the discussion of the strategies of residents toward their offspring. Trivers (1972:139) wrote
that parental investment was “any investment by the parent in an individual offspring that
increases the offspring’s chance of surviving (and hence reproductive success) at the cost of
the parent's ability to invest in other offspring.” So defined, parental investment includes the
metabolic investment in the primary sex cells but refers to any investment (such as feeding or
guarding the young) that benefits the young. It does not include effort expended in finding a
member of the opposite sex or in subduing members of one’s own sex in order to mate with a
member of the opposite sex, since such effort (except in special cases) does not affect the survival
chances of the resulting offspring and is therefore not parental investment.”
The two essentials specified in Trivers’ definition are increased success of offspring and parental
cost in the form of restriction of the parent’s further reproduction. Suppose, however, that we
view parents as producing offspring as a means of transmitting parental alleles into the future,
rather than as ends in themselves. From this perspective it is possible to think of both investment
in offspring (Trivers meaning) and investment of offspring. In the latter sense a parent might
“invest” an offspring in perpetuation of parental alleles at the natal site (this could be called
philopatric investment of the offspring) or in disseminating those same parental alleles to other
locations (this could be called disseminative investment). In unstable environments parental
fitness could well depend on the mix of the two. If parents do in fact behave so as to determine
the fates of offspring, as I argue below, they are the effective agents in both types of investment,
and both are therefore “parental.”
Reviewers have argued cogently that Trivers’ original meaning should be kept clear (a sen-
timent with which I concur), and thus I have endeavored to find some alternative term by which
to refer to parental investment of young. Although no totally satisfactory term has turned up, I
will refer, in those cases where a specific term is convenient, to the process of allocation of young
to philopatry or emigration through parental acts as parental disbursement. One important
Starting Points 7
difference between parental investment and parental disbursement is that in the former, as
defined by Trivers (1972), parents invest in offspring at a cost to further parental reproduction.
In parental disbursement, expulsion of offspring may facilitate further parental reproduction.
Practical Aspects of Categorization
. Applying a set of coherent and consistent definitions to the categories of animals involved in
dispersal is difficult on paper and still more difficult in the field. Residents are commonly defined
as individuals repeatedly captured in live traps at a set of stations within a sampling area (typically
a trapping grid) for a specified length of time, or simply as any animal captured one or more
times at the same or closely associated stations on an area designated as a “control” grid (e.g.,
Reich and Tamarin, 1980). The method positively identifies some proportion of residents. The
uncertainties lie in the proportion of residents detected, and the proportion of non-residents
included. Such samples may be highly biased because conventional live traps might not ade-
quately sample the individuals present. Boonstra and Krebs (1978) and Beacham and Krebs
(1980) found that close to 50% of Microtus present in areas trapped concurrently with conven-
tional live traps and pitfall traps were caught only in the pitfalls. Overall, eight times as many
voles were caught in pitfalls as in conventional traps, and the pitfall sample was biased toward
smaller, faster-growing individuals. In enclosures more males than females avoided live traps
and males that avoided live traps did so over a longer period.
Establishment of practical conventions for identification of non-residents (inclusive of emi-
grants, transients, and immigrants) has proven especially difficult. Identification of emigrants on
the basis of simple disappearance (Hilborn, 1975) does not discriminate between emigration and
death in situ. Other than disappearance, the most common criterion for non-resident status has
been capture on a plot from which residents have been removed (e.g., Joule and Cameron, 1975;
Krebs et al., 1978; Krohne and Miner, 1985; Myers and Krebs, 1971; Reich and Tamarin, 1980;
Reich et al., 1982). The problems with this approach lie in the numerous unjustified assumptions
and the superficial interpretations that have prevailed. All individuals encountered in such a
‘vacuum’ have been assumed to have emigrated at some previous time and have been regarded
as representative of emigrants. Transients have not, in most cases, been distinguished from settlers.
Unless provision is made for a correction (e.g., Baird and Birney, 1982a) such samples may
include an unknown proportion of residents making sorties outside neighboring home ranges.
Initially, removal grid samples may also include a high proportion of individuals that were
previously present but invulnerable to trapping (Verts and Carraway, 1986). Consideration of
the evidence leads me to the conclusion that the individuals captured on removal grids are a
mixed bag of nearby residents, transients, settlers, and immigrants. Most appear to be derived
from a pool of transients whose origin and past experience are unknown. It is an enormous leap
of faith to assume that a removal grid sample is representative of any specific group of individuals
at the time they emigrated.
Misinterpretation of the removal grid results has been most serious where the intention was
to compare philopatric and emigrant individuals originating from a nearby control plot and
measure emigration rates. Even if the settler-transient component is clearly discriminated, it
need not represent the original emigrant set from which it was derived. Age-specific weight,
reproductive status, wounding, and aggressiveness of transients are likely to have been altered
in transit, either through change in the individuals themselves (growth, experience, maturation),
settlement elsewhere, habitat choice, or mortality. Further bias could result from interaction
among settlers, so that they are even less likely to be representative of emigrants than are the
members of the transient pool. The origins of transients could be diverse in time, distance, and
habitat, and are likely to be unknown; most transients could have originated at distant localities.
The transient pool may be so large as to lead to gross overestimates of emigration rate. Boutin
et al. (1985) compared emigration rate of arctic hares (Lepus sp.) as measured from radio-
collared individuals with that obtained by the removal grid approach. They showed that the
removal grid estimate of emigration rate was approximately 28 times too high.
8 Rodent Dispersal
Removal grids do not simulate immigration into an established group (Dueser et al., 1981,
1984). To remedy this Dueser et al. (1981) attempted to identify a non-indigenous component
in unmanipulated populations, proposing that all individual voles first entering the trappable
population above a specified body weight could be assumed to have originated external to the
trapping grid. Their results, like those of Boutin et al. (1985), imply that there may often be a
very large pool of transient individuals. For identification of emigrants, the approach of Dueser
et al. (1981) is subject to most of the same deficiencies as the removal technique. Like the latter,
it is also open to question if it relies solely on live traps to which all categories of individuals
may not be equally vulnerable (Andrzejewski and Rajska, 1972; Beacham and Krebs, 1980;
Crowcroft and Jeffers, 1961; Gliwicz, 1970). It can be criticized as well on the grounds that the
body weight criterion is unacceptably arbitrary (Tamarin, 1984). Growth rates might vary
seasonally (Schwarz et al., 1964) and, as Sauer and Slade (1986) have emphasized, seasonal
patterns of change in growth rate make mass a poor predictor of age in voles. Further, Bietz et
al. (1977) have shown that voles may suffer differential weight loss in live traps.
Identification of transient individuals by use of drift fences is subject to similar difficulties.
Verner and Getz (1985) concluded that most individuals passing through gates in a fence were
resident on adjacent home ranges. The use of enclosures with exit doors to identify emigrants
(Gaines et al., 1979b) has the advantage that the origin of the sample is known. One then only
needs to discriminate between true emigrants and residents making sorties beyond their normal
home ranges, but this is not easily accomplished. Singleton (1985) found that many Mus caught
in “exit” traps in fences around haystacks subsequently re-entered the haystacks.
Methods based on travel of individuals across, or occurrence in, atypical or unsuitable habitat
(Beacham, 1979a; Hestbeck, 1986; Pickering et al., 1974; Tamarin et al., 1984) are subject to a
bias through variations in willingness to enter the atypical habitat, enclosure effects, and the
problem of unknown origin and history of the transients so identified. The filter-cropping system
used by Hestbeck (1986) resulted in the classification of most large male Microtus californicus
as emigrants, perhaps because they tended to make forays outside their ranges. Beacham (1979a)
and Beacham and Krebs (1980) combined a mowed boundary strip with both pit and live trapping
in an enclosure. Their results were encouraging: the sample of individuals that crossed the
boundary strip was biased toward those vulnerable to pit traps. Thus the live-trap sample was
biased toward sedentary individuals, the pit-trap sample toward emigrants.
Each of the techniques discussed above has merits as well as deficiencies. In part the problem
has been one of not giving sufficient critical thought to what each technique does or does not
do. The best approach might be through stepwise designs that begin by discriminating individuals
that are fully resident and those that are not. Residents might be clearly identified through
displacement of individuals over short distances from which those that had established residency
would be expected to home. To my knowledge this approach has not been tested.
Even if resident and non-resident categories can be clearly distinguished in nature, the problem
of discriminating between philopatric individuals and emigrants remains. To solve it, definitions
must be clearly formulated. Distinctions that are based on two or more criteria will be desirable
(Tamarin, 1984). Radio-tracking and isotope marking possibly have the greatest promise for
identifying instances of emigration and, thus, the emigrants themselves.
Ultimately non-residents, emigrants, and non-emigrants should be discriminated within specific
cohorts and even litters. Similarly, precise techniques must be devised to discriminate among
transients, settlers, immigrants, and residents on exploratory forays.
Baseline Observations
Site fidelity is strongly developed in rodents. If established residents are experimentally dis-
placed, they generally return to their home ranges, or appear to attempt to do so (Anderson et
al., 1977; Bovet, 1980; Griffo, 1961; Murie, 1963; Robinson and Falls, 1965; Stickel, 1968).
Settlement of displaced residents at a distant release site has been observed only rarely (e.g.,
Starting Points 9
Bovet, 1980). Home ranges appear to be important commodities to which young rodents must
aspire.
Each rodent is born on the home range of its female parent but not necessarily within the
home ranges of any other conspecifics. The common factor for all rodents is that life begins in
the context of the mother-young unit and the maternal home range. This natal range has proven
itself adequate for maintenance and reproduction, and is inhabited by one or more relatives
that might benefit by altruistic behavior toward the young born there. Young might establish
themselves with minimal risk and effort within the maternal range.
Most young that survive and reproduce appear to do so within a short distance of the natal
site. The effective dispersal distances (sensu Shields, 1982) so far reported in rodent populations
are not very great. Even if data are biased in favor of short dispersal distances, the high frequency
of short distance movements is still significant. Because rodents appear physically capable of
traveling great distances, the evident high frequency of philopatry and the predominance of
very short dispersal distances suggest that rodents have philopatric tendencies and that emigration
requires a causal explanation.
Fitness: What and for Whom?
Horn (1983) observed that natural selection within populations seems likely to be biased against
emigration. In environments where local populations are exterminated, however, only individuals
that leave their natal site can exploit the vacated habitats and found new populations. Horn
illustrated his point by reference to the situation described by Gill (1978) in the red-spotted newt
(Notophthalmus viridescens). Although the patchiness of rodent habitats is less obvious than that
of pond dwelling newts, rodent habitats might be similarly discrete, the cost of moving between
them could be similar to that for newts, and the stability of rodent environments could be
considerably less than that of the lakes in which newts spend their early larval and adult stages.
If we assume that local populations exist as discrete units, and that there is great variation in
survival and reproductive success of these units, it is evident that there may be a selective
advantage in dispersal. We must ask, however, whether the advantage lies with the “metapop-
ulation,” local population, resident parent, or emigrant offspring.
As suggested by Gaines and McClenaghan (1980), theories proposed to explain the evolution
of dispersal phenomena in rodents can be categorized on the basis of whether they see selection
as generating differential fitness among individuals (e.g., Murray, 1967) or among populations
(e.g., Van Valen, 1971). The currently prevailing view is that evolution operates primarily, if
not exclusively, on the basis of selection among individuals. In this essay I have focused primarily
on questions of loss and gain in individual fitness and follow Stenseth (1983) in defining individual
fitness as the relative number of successful offspring.
Fitness for whom? My focus on individual fitness does not resolve the question in favor of
resident or emigrant, nor does it preclude examination of the implications for differential evo-
lutionary success of lineages or local populations. The next chapter examines the assumption that
emigrants gain fitness.
II
THE EMIGRANT FITNESS HYPOTHESIS
The expressed or implied assumption in numerous influential publications dealing with dispersal
in rodents has been that emigration occurs because there is, on average, a gain in fitness to
individuals that emigrate (e.g., Bekoff, 1977; Chitty, 1967; Fairbairn, 1978a, Holekamp, 1984;
Holekamp et al., 1984; Howard, 1960; Krebs, 1978a, 1978b, 1979; Krebs and Myers, 1974;
Lidicker, 1962, 1975, 1985b; Murray, 1967; Myers and Krebs, 1971; Tamarin, 1978). Much theory
and many years of empirical investigation have been based on this assumption.
The belief that dispersal phenomena in rodents have evolved through gain in fitness to emigrants
is the essential point of what I refer to hereinafter as the Emigrant Fitness Hypothesis (EFH).
I think it is erroneous. It is therefore approprite to examine the assumptions that underlie the
EFH, consider the possible criteria for its falsification, and critically review the supporting
arguments in the light of the available evidence.
Assumptions of the EFH
The first assumption of the EFH is that there is inherited variability in tendency to emigrate.
The second assumption is that this variability exists in populations because the ancestors of
individuals carrying alleles favoring emigration have gained fitness as a result of their expression.
Phenotypic expression of the relevant alleles has been supposed to be either spontaneous (Howard,
1960) or responsive to environmental conditions and stimuli (most other authors).
Suggested mechanisms by which emigrants gain fitness include a higher probability of survival,
access to higher quality habitat, contact with more conspecifics with the possibility of more
frequent matings, wider dispersion of genetic material, greater fitness of offspring through an
increase in heterozygosity, higher probability that offspring would have new and desirable genetic
combinations, and avoidance of competition or of population crashes through departure from
crowded habitats (Lidicker, 1962).
Falsifiability of the EFH
The EFH is not easily falsified. We can neither prove the non-existence of alleles programming
individuals to emigrate spontaneously nor the non-existence of stimuli when emigrants depart
from a natal site. We can, however, ask whether emigrants gain or lose fitness. If it can be shown
that, on average, emigrants lose fitness the hypothesis is disproven. If we find no evidence that
emigrants differ genetically from non-emigrants, and discover that the arguments for a gain in
fitness by emigrants are illogical, are opposed by the bulk of available evidence, or both, the
EFH comes under grave suspicion. If an alternative can be offered that provides a better
explanation of the evidence, the case against the EFH is strengthened even though an hypothesis
with a better fit to the data does not constitute disproof. In the following discussion I will consider
the processes that have been supposed to lead to increased fitness for individuals that emigrate,
beginning with the arguments for increased survival through emigration.
Increased Fitness Through Emigration: Survival of Emigrants
How do survival rates of philopatric and emigrant young compare? Philopatry has advantages
that may contribute to survival (Michener, 1981). Emigrants lose these advantages. Does the
average gain offset the average cost? Although the data are biased by the greater technical
difficulties of measuring survival rates of the individuals that leave their natal sites (especially
those individuals that move long distances), studies of populations of rodents and other small
10
Emigrant Fitness Hypothesis 11
mammals equate a high probability of survival with philopatry and a lower probability of survival
with emigration (e.g., Cockburn and Lidicker, 1983; Michener, 1981; Smith and Ivins, 1983).
In the only direct comparison I have found, survival of Dipodomys spectabilis that settled on
the natal site was 50% higher relative to those that established themselves away from the natal
site (Jones, 1986).
. What is the immediate (pre-establishment) effect of emigration on survival? When an indi-
vidual emigrates it must, for some period, become a transient. Survival rates during the travel
period are critical to the argument for the EFH. The activities and fates of transient individuals
are difficult to monitor; there is need for much more investigation of transients and their destinies,
but the information available is consistent. Experimental studies (e.g., Ambrose, 1972; Metzgar,
1967) indicate that unestablished voles and mice are more vulnerable to predators than are
residents. Observational approaches lead to the same conclusion. High disappearance rates of
juvenile and yearling male Richardson’s ground squirrel correlate with their relatively greater
movement, and loss to predators appears to account for the high female bias in adult sex ratio
in ground squirrels (Michener and Michener, 1977; Schmutz et al., 1979). Errington (1943, 1946,
1963), in his analyses of muskrat mortality, showed that most individuals killed or consumed by
mink were either transients, or present in peripheral and inferior habitats. Errington argued that
death of transients was so highly probable as to approach the inevitable. Korpimaki (1985)
attributed the male bias among voles caught by kestrels to wider and more frequent movements
of that sex. Pielowski (1962, cited in Petrusewicz, 1966) found that European vipers preyed
selectively on unestablished mice and voles. Young rodents (potential emigrants) are character-
istically over-represented in prey of raptors (e.g., Beacham, 1979c). Myllymaki et al. (1962)
observed that transient Lemmus remained in the open, behaving aggressively toward human
observers (and presumably other formidable potential predators), but residents in similar situ-
ations quickly took cover. Despite the conclusion that the aggressive behavior of transients might
have adaptive value in some encounters, the observation supports the concept of transient
vulnerability.
Many factors are likely to contribute to lower survival of transient animals. Lack of access to
prepared runways may increase vulnerability to a variety of stresses, as well as to predation.
Numerous other studies (e.g., Beacham, 1979a; Bergeron, 1980; Boonstra, 1977a; Frank, 1957)
concur on the relative vulnerability of unestablished microtines to predation, disease, and incle-
ment weather. Beacham and Krebs (1980) found that Microtus townsendii caught in pitfall
traps (a sample biased toward unestablished individuals) had more wounds and a higher incidence
of botfly infestation than did a live-trap sample.
By definition, transients must spend time in unfamiliar areas. It is reasonable to assume that
when traversing unfamiliar terrain, survival of transients may be affected by the efficiency with
which they are able to find and utilize food and cover. Kozakiewicz (1976) attributed lower
mean body weight of transient Clethrionomys to poor nutrition and to exposure due to lack of
prepared nesting sites. Vulnerability of emigrants also may be significantly affected by social
status. Presumed transients are commonly found to be socially subordinate to residents (e.g.,
Fairbairn, 1978b; Myers and Krebs, 1971). Subordinates tend to avoid resident conspecifics
(Armitage, 1974; Clough, 1968) and may thereby lack access to resources (Baird and Birney,
1982b; Calhoun, 1963; Noyes et al., 1982). Access to resources bears on survival in many ways.
Daan and Slopsema (1978) found that per-capita risk of kestrel predation was least at times when
the number of active resident voles was greatest. Because subordinate rodents tend to time their
activity to avoid dominants (Calhoun, 1963), unestablished individuals may be more vulnerable
to predation as a result of shifts to less favorable activity cycles. Subordination to dominants may
also imply habitat in which vulnerability to predators is increased. Spencer and Cameron (1983)
found that Sigmodon hispidus inhabiting patches with less cover were subordinate to individuals
inhabiting patches with better cover (their study, however, failed to reveal a significant difference
in survival rates). Roberts and Wolfe (1974) produced some contrary evidence as to vulnerability
to predation. In a room in which cotton rats were exposed to predation by either a domestic cat
12 Rodent Dispersal
or ared-tailed hawk, subordinate rats were taken most frequently by the hawk, whereas dominants
were more often taken by the cat.
Socially subordinate cotton rats are less likely than dominants to enter either baited traps or
traps scented by dominants (Summerlin and Wolfe, 1973). In large outdoor enclosures subordinate
male Mus were less likely than dominants to occur at sites where food was provided (Noyes et
al., 1982). Tardiff and Gray (1978) found that resident Peromyscus leucopus were food specialists,
whereas immigrants were food generalists. Thus transients may find food less efficiently, spend
more time seeking it, and as a consequence be more likely to be caught by predators.
Results of concurrent trapping with pit traps and conventional live traps (Andrzejewski and
Rajska, 1972; Beacham and Krebs, 1980; Boonstra and Krebs, 1978) showed that unestablished
voles are less vulnerable to baited live traps than are residents. Captures in pitfall traps sometimes
increase sharply at the time when emigration tends to be most pronounced, although this might
vary interspecifically (Boonstra and Rodd, 1983, 1984). Differential vulnerability to pitfall and
baited traps may have several non-exclusive explanations. Baited traps may soon become marked
by the scent of residents, particularly when traps are left in place between sampling periods. A
significant possibility is that transients are less likely to investigate and utilize unfamiliar food
sources, either because they lack the confidence to do so, or because confrontations with dominants
are avoided and habitats with food and cover are occupied by resident conspecifics. If low
vulnerability to baited traps reflects low foraging efficiency, high vulnerability to pitfall traps
could indicate that transients are accident prone; accidental death or injury in unfamiliar en-
vironments could contribute to the low survival of transients (Errington, 1948, 1946).
Andrzejewski and Wroclawek (1961) found that transient voles succumbed more readily than
residents to the stress experienced in live traps. A transient individual might be physiologically
less competent than it would be if it were established on a home range. Any nutritional stress
would be expected to increase vulnerability to climatic extremes. If an individual has become
transient as a result of defeat in an agonistic encounter, further defeats are probable (Anderson
and Hill, 1965). Adrenal function can be impaired as a result of repeated defeats (Archer, 1970;
Vale et al., 1970). Social subordinates are likely to be physiologically stressed (Christian, 1963)
and puberty, in itself, is a time of physiological stress for most individuals (Seabloom et al., 1978;
Seabloom, 1985), thus compounding the total stress experienced by transients.
Summarizing, the material reviewed above includes experimentally and observationally doc-
umented vulnerability of unestablished individuals to predation as well as considerations that
are more tenuous and largely unexplored. It implies clearly that transiency and lowered survi-
vorship are correlated, and, thus, that individual fitness rarely will be increased by high survival
during transiency, regardless of habitat. Logically, a transient can be expected to spend at least
some time in habitat that is less than “suitable” so as soon as an individual emigrates it enters a
high-risk (transient) category. Except in cases where the site of origin has become physically
uninhabitable, I have not found evidence indicating that transient existence per se increases the
probability of survival. The total risk depends on the duration of transiency, but survivorship of
transients seems inadequate for selection of alleles that promote emigration behavior.
Increased Fitness Through Emigration: Avoiding Competition
The tenets of the EFH with respect to competition can be stated in various ways. It may be
implied or explicitly stated that emigrants leave to avoid competition, that competition induces
emigration, that emigration leads to reduced competition, that emigrants gain fitness as a con-
sequence of this reduction in competition, or that the reduced competition cost experienced by
emigrants selects for emigratory tendency. Still another possibility is that emigrants contribute
to the success of relatives by their departure.
Murray (1967) argued that as philopatric young would face parental competition for food and
shelter, young might gain fitness by emigrating. Similarly, Brown and Gibson (1983) supposed
that a more distant location is always likely to be more favorable than the exact birthplace, in
Emigrant Fitness Hypothesis 13
part because distant locations would be free of parental and sibling competition. Moore and Ali
(1984) concluded that most intersexual differences in the probability of emigrating were due to
differences in intrasexual competition, and that competition underlies mammalian patterns of
emigration in general. Dobson (1982) and Dobson and Jones (1985) argued that competition did
not explain all mammalian dispersal patterns, but granted it an important role. Trivers (1974)
pointed out that offspring are likely to lose in competition with parents, and that offspring
succeeding in maximizing their own reproductive success at the natal site might be doing so at
the expense of parents or siblings sharing similar genotypes and thus incur a cost in inclusive
fitness.
It is clearly logical that competition among siblings and between parents and offspring can
occur, and that fitness could be increased when competition is avoided. It is logical, as well, to
postulate that young might be less effective competitors than fully grown individuals; this will
be considered in greater detail in later sections. It is also possible that genetic similarity of parents
and their offspring might intensify competition. Although parent-offspring conflict has not been
intensively studied in rodents, all of the above appear to be reasonable arguments. Such consid-
erations do not demonstrate, however, that an emigrant offspring departs the natal site in order
to avoid competition, that it will encounter less competition if it leaves the natal site, or that it
is the avoidance of competition on the part of the emigrants through which selection operates.
The fundamental point is whether competition becomes more or less severe when an individual
emigrates. Despite the issues raised above, and contrary to the EFH, there are strong reasons to
expect that an emigrant should anticipate more competition, and more damaging competition,
as a result of departure from the natal site. As distance away from the natal site increases,
relatedness presumably decreases. Parents and other close relatives have a vested interest (the
potential gain through inclusive fitness) in the welfare of potential emigrants. Restraint may
temper competition among relatives or familiar individuals, all of whom may behave altruisti-
cally. As a transient moves into a new area, competitive interactions with residents are not likely
to be buffered in this way. More distantly related conspecifics resident in other habitats will lack
any incentive for restraint, and will compete unreservedly in their own interest and the interests
of their own relatives. By this argument both interference and resource competition could increase
away from the natal area. Simultaneously, the potential immigrant, as a result of lack of familiarity
with the area, is likely to be at a competitive disadvantage. Intruders, almost without exception,
are approached aggressively, and defeated, by residents (Petrusewicz and Wilska, 1959).
There is evidence for this argument that competition may be significantly restrained at the
natal site. Brown and Brown (1984) have shown that in the more communal jays, parents may
increase their own fitness by facilitating inheritance of the natal site by their offspring. Davis
(1984) found that those female Spermophilus richardsonii that associated with near relatives
shared more of their core area with neighbors, spent more of their time feeding, spent less time
in aggressive interactions and vigilance, and had higher breeding success than those not so
associated. Although prairie dogs do not appear to discriminate between close kin (offspring, full
sibs) and other kin (half sibs, nieces, nephews), and although the degree of nepotism varies with
the intensity of competition, both sexes interact more amicably with kin than with non-kin
(Hoogland, 1986). Yellow-bellied marmots show higher rates of cohesive behavior and greater
overlap of foraging areas among closely related individuals (Armitage and Johns, 1982).
Irrespective of relatedness, it appears that familiarity, per se, is likely to buffer competitive
interactions. Deer mice are less aggressive toward neighbors than toward strangers (Healey, 1967).
In the laboratory familiar Acomys are more likely to share food and huddle together than are
strangers (Porter et al., 1980, 1981).
Even before site-specific dominance is fully established, a potential emigrant may be a more
effective competitor on the natal range than it would be on unfamiliar terrain. I know of only
one study in which access to resources, as determined by competition, can be compared before
and after dispersal. Unfortunately the study was done in an enclosure so that the dispersal option
was limited, but the results still merit consideration. Calhoun (1963) studied a population of
14 Rodent Dispersal
Rattus norvegicus of wild stock in a large enclosure with a central food distribution area. The
introduced parent stock settled and bred close to the food source. Emigrants moving out from
it lost rank in competitive interactions. Their access to the central food source was reduced, and
reproduction declined or ceased.
Some transients must eventually discover suitable habitat that is either vacant or characterized
by low density. Because rodents interact socially, however, one can assume neither that com-
petition is directly proportional to density nor that fitness is inversely proportional to density, as
the competition argument seems to imply. Competition is a relative phenomenon.
I conclude that competition may well exist at a natal site, but is likely to be more intense and
less benign elsewhere. As Greenwood (1983) has said, there is considerable evidence that the
advantages of philopatry to young may often outweigh any costs of competition that are specific
to the natal site. The argument that selection might operate to create emigratory tendencies
because emigrants gain fitness as a result of reduced competition overlooks important mitigating
factors present in philopatry, evidence that competition may be more intense elsewhere, and
the low probability of finding unoccupied habitat.
Increased Fitness Through Emigration: Opportunity for Breeding
Emigration might lead to increased fitness if it were a prerequisite for reproduction, or if
transients contacted more potential mates, mated sooner, or mated more often than non-emigrants
(Lidicker, 1962). All of these consequences are possible. Emigration exposes individuals to en-
vironmental change and such change may be a reproductive stimulus. Laboratory experiments
have shown that social and other changes in environmental conditions can serve to break down
reproductive inhibitions in confined Mus colonies (Crowcroft and Rowe, 1958; Petrusewicz,
1963). Sheppe (1966) found that introduction of Peromyscus leucopus to uninhabited islands
induced unseasonal breeding.
Laboratory studies raise the possibility that philopatry may cause puberty to be delayed. In
confinement, continuous close association with conspecifics delays puberty in Meriones ungui-
culatus (Agren, 1981, 1984a), Peromyscus maniculatus (Dewsbury, 1982c; Hill, 1974; Terman,
1980), Microtus californicus (Lidicker, 1979), M. ochrogaster (Carter et al., 1986; Getz and
Carter, 1980; Hasler and Nalbandov, 1974; McGuire and Getz, 1981; Richmond and Stehn,
1976), M. pinetorum (Schadler, 1983), and Mus musculus (Drickamer, 1974; Massey and Van-
denbergh, 1980). In most cases the effect is due to pheromones produced by members of the
same sex. If similar inhibition occurs in nature in these species, emigration might release mat-
uration, resulting in earlier reproduction (Carter et al., 1986). Bronson (1979) has specifically
suggested that the pheromone system that influences puberty in Mus musculus could have evolved
as a result of its effectiveness in promoting colonization.
In a polygynous species suppression of puberty in males could, at least in the abstract, deprive
the inhibited individual of a large number of possible matings. The reduction in number of
matings would be less if the mating system is monogamous, but the proportion could be the
same. For females the potential effects would be equivalent irrespective of mating system. Because
the number of litters a female can bear has a physiological limit, delayed mating may limit the
number of young primarily through the restriction set by the length of the breeding season.
Is inhibition of maturity by parental pheromones a mechanism that favors breeding through
emigration? If suppression of puberty by the direct effect of adult pheromones were to enhance
fitness through emigration, two requirements must be met: exposure to same-sex adults must be
sufficient to induce suppression in unconfined natural populations and potential emigrants must
respond to suppression by emigrating. Evidence on the first point is suggestive, but scant and
equivocal. Lidicker (1979) observed inhibition of maturity in Microtus californicus housed in
small outdoor enclosures. Wasser and Barash (1983) and Armitage (1986b) reported evidence
suggestive of such inhibition in marmots.
King (1983) proposed a “mate search hypothesis” to explain emigration, based on the as-
sumption that emigration would shorten the time to first reproduction. He suggested that at
Emigrant Fitness Hypothesis 15
sexual maturity Peromyscus and other small rodents leave the natal area to search for mates. As
potential mates are generally available at the natal site, arguments for King’s hypothesis, and
for earlier or more frequent mating through emigration, presume either delayed maturity or
postmaturity bars to philopatric mating. The key assumption in King’s hypothesis is that an
individual would respond to the lack of a mate by traveling in search of one. This does not seem
to happen. Howard (1949) observed that when one member of a breeding pair of P. maniculatus
disappeared the other member might remain on the home range for many months without a
mate. Jannett (1982) has observed similar behavior in Microtus montanus. Getz et al. (1987)
observed the breakup of 98 monogamous pairs of M. ochrogaster and determined that only 11%
of the surviving partners acquired new mates. Carter et al. (1986) stated that in such cases it
was rare for a survivor to move and establish a breeding unit elsewhere. Because these observations
relate to residents that have lost mates they are, however, not direct tests of King’s suggestion
that pubertal young might emigrate in search of mates.
The evidence as to breeding condition of transient young is ambivalent. Fairbairn (1978a)
found that Peromyscus maniculatus emigrating during the breeding season were “mainly light
weight non-breeding males’ and that less than 25% of either female recruits, or female transients,
were in breeding condition when they first entered the trappable population. Myers and Krebs
(1971), in contrast, reported that the proportion of small male Microtus townsendii with scrotal
testes was higher on a removal grid than on the control.
Are transients in breeding condition likely to breed? The probability that an individual will
mate is likely to depend on social rank. Although most tests of aggressiveness have been carried
out in “neutral” arenas and should be sceptically evaluated, there are grounds for assuming that
residency is likely to be associated with dominant status and non-residency with subordinate
status (e.g., Turner and Iverson, 1973). Social subordination has repeatedly been directly asso-
ciated with impairment of sexual function (Bronson, 1976; Bronson et al., 1973; Calhoun, 1962a,
1962b; DeFries and McClearn, 1970; Dewsbury, 1981; Huck and Banks, 1982a, 1982b; Singleton
and Hay, 1983; Vale et al., 1970). Dominance and aggressiveness are positively correlated with
body weight (Brenner et al., 1978; Reich et al., 1982). Comparison of body weight of resident
and transient individuals has been confused as the result of the difficulty in consistently deter-
mining residency status, as well as by failure to take seasonal trends in growth and movement
into account. However, if non-residents are lighter (Boonstra and Krebs, 1978; Fairbairn, 1978a,
1978b) and socially subordinate to residents (Christian, 1970; Fairbairn, 1978b; Healey, 1967;
Krebs et al., 1978; Mackintosh, 1978; Myers and Krebs, 1971; Petrusewicz and Wilska, 1959;
Spencer and Cameron, 1983), they are unlikely to dominate heavier competitors and usurp ranges
or mating rights. The most appropriate tests of the relationship between residency and dominance
so far published (Wolff et al., 1983) support the prediction that even if they are not heavier,
residents are likely to be dominant over non-residents as a consequence of residency itself. Resident
Microtus ochrogaster males drive off transient males (Carter et al., 1986) and resident Marmota
calligata males were invariably successful in driving off intruders in 41 encounters (Barash, 1981).
Subordinate males are also less effective than dominants in pheromonal activation of sexual
activity in females (Lombardi and Vandenbergh, 1977). Although there are species differences
(Bronson, 1963), successive exposures to more aggressive individuals can make less aggressive
individuals progressively more timid.
Dewsbury (1981) found that prior residence, dominance, and greater mating success were
correlated in deer mice, Peromyscus, in a laboratory situation. Singleton and Hay (1983) found
that subordinate males sired fewer litters than did dominants in enclosed Mus populations. In
another confined population of house mice, R. J. Wolff (1985) noted that only the founding
dominant male bred initially. Subsequently only those males that came into possession of territories
bred. In a seminatural experimental environment, dominant male Mesocricetus auratus produced
more offspring than subordinates (Huck et al., 1986).
Female preference may lower the probability that transient males will mate. In laboratory
tests Shapiro and Dewsbury (1986) found that female Microtus ochrogaster preferred dominant
16 Rodent Dispersal
males to subordinate males. However, female M. montanus failed to show preference. As long
as female rodents mate preferentially, socially subordinate transient males are unlikely to compete
successfully with resident males or to be as acceptable to resident females as are resident males
with which they have mated previously (DeFries and McClearn, 1970; Huck and Banks, 1982a,
1982b; Mihok, 1981; Singleton and Hay, 1983; Webster et al., 1982). Kawata (1985b) found that
all Clethrionomys litters for which he determined paternity were sired by males that were
resident. However, Farentinos (1980) observed that unconfined female tassel-eared squirrels
(Sciurus aberti) sought out and mated with subordinate males.
Even if transient males are unlikely to mate, the crucial test is whether philopatric males mate
sooner than those that emigrate. There is little evidence as to how long a transient might wander
before settling. Kozakiewicz (1976) found that the average age of transient Clethrionomys
glareolus was 4-6 months. Cohorts born early in the breeding season predominated, indicating
that animals that emigrated were slow to settle and thus slow to breed. I expect that the interval
between emigration and immigration will be highly variable, especially in males, and will be
influenced by habitat patchiness, season, and population density.
One exception to sedentarity in breeding males might exist in Richardson’s ground squirrels
in which females are philopatric but adult males rarely occupy the same area in two successive
breeding seasons (e.g., Michener, 1980, 1983b). However, even this does not appear to be an
invariable characteristic (Davis and Murie, 1985). Further, there seems to be no evidence as to
whether males that move succeed in breeding in subsequent seasons. At present it appears that
male transients are unlikely to breed and, thus, that transiency delays breeding. Males are unlikely
to decrease time to first reproduction, or frequency of mating, through emigration.
Some aspects of transiency may reduce chances of mating in both sexes. As suggested above,
lighter weight may indicate that as social subordinates transients may be less able to find food
and more inhibited in approaching it (Calhoun, 1963). Females are likely to be especially sensitive
to inadequate nutrition, which is a bar to sexual activity (Batzli, 1975; Cooper and Hayes, 1967;
Sinclair, 1975; Strecker and Emlen, 1953). Spencer and Cameron (1983) found that reproductive
success was lower in subordinate cotton rats occupying patches in which cover had been exper-
imentally reduced. Tamarin et al. (1984) noted that most female Microtus caught in atypical
(forested) habitat were non-reproductive.
It appears that establishment on a home range may be the crucial prerequisite for attainment
of puberty in some species (Bujalska, 1973; Sadleir, 1965). It would be useful to know whether,
as in the case of Microtus ochrogaster, transient females are generally unacceptable to resident
males, and whether spatial and social establishment of females are consequences of mating or
prerequisites to mating.
With the exception of Bujalska’s (1973) study we have little field data on the relationship
between establishment and first pregnancy. Bronson (1979:291) concluded on the basis of a
review of literature on pheromonal cueing in the house mouse that “only after establishing a
home in an adult male’s territory ... will the young female attain her pubertal ovulation with
any degree of efficiency.’ Because successful rearing of a litter commonly requires construction
of a nest or burrow, and demands access to food resources adequate to support gestation and
lactation, female sedentarity should precede or be coincident with the later stages of pregnancy.
With few exceptions (e.g., Myllymaki, 1977a) transient females have not been found to be
pregnant.
As suggested by Morris (1982), it seems likely that time spent as a transient delays mating and
represents a loss of reproductive value. Despite the laboratory data showing that the maturation
of philopatric young may be delayed, the balance of the evidence weighs against the hypothesis
that transients of either sex might mate sooner or more frequently than non-emigrants. Sexual
maturity is commonly a stimulus to, and prerequisite for, emigration (King, 1983). An “early
mating’ interpretation of puberty suppression appears to make contradictory assumptions: that
juveniles must mature in order to emigrate, and that they cannot mature until they have
Emigrant Fitness Hypothesis 17
emigrated. I believe we will eventually discover that the adaptive value of suppressed puberty
lies in delaying emigration, rather than stimulating it.
Increased Fitness Through Emigration: Immigration and Breeding
In the previous section I examined the probability that the act of emigrating and becoming
a transient would lead to earlier or more prolific reproduction. Here I turn to examination of
the process of immigration.
Recall that in the first chapter a distinction was made between settling and immigration. We
do not yet know whether settlement is a separate process that must be completed before repro-
duction can begin. Do transients choose unoccupied areas or do they attempt to settle near
conspecifics? Is choice of site influenced by availability of a mate? If a male or non-pregnant
female settles in unoccupied habitat, reproduction will be delayed until a mate appears. Settling
in an established group may avoid the problems of finding or waiting for a mate, but it requires
acceptance by residents. Does relatedness of the settler have a bearing on acceptance? Does
acceptance entail some delay in breeding?
Agren (1984b) observed the founding of experimental colonies of Meriones unguiculatus in
detail. Males first established themselves in unoccupied areas and females then selected males
and/or territories and became aggressive toward other males. We do not know if this pattern
characterizes settling in unoccupied areas in other species.
As subordinates, transient males appear most likely to settle where no resident male is present.
Insuch locations females are likely to be less abundant. Bronson (1979) concluded on physiological
grounds that young male house mice arriving in a suitable but unoccupied habitat were likely
to be in poor reproductive condition. If this is true, delay in the arrival of a mate is not necessarily
wholly disadvantageous, deferring competition for mates and allowing time for physiological
recovery. On the other hand, transients can become reproductively active quickly after settling
in unoccupied habitat. Krebs et al. (1978) concluded that animals taken on removal grids were
at least as mature reproductively as were residents on a nearby control grid.
A transient could settle in a recently vacated home range, as opposed to settling in a wholly
vacant habitat. Vacancies might be taken up quickly. Price et al. (1986) reported that resident
Tamiasciurus were replaced within hours by new arrivals. The new territories duplicated those
of the former residents.
Although Bovet (1978) estimated that 30% of the woodmice (Apodemus sp.) that he displaced
settled in the vicinity of the release site, experimentally displaced residents usually do not settle
but instead return to their former home ranges. Homing success can vary with habitat (Anderson
et al., 1977), but there is much evidence that homing is more advantageous for displaced residents
than is settling in the areas where they are released. This probably is because transients cannot
readily penetrate established groups. Dahl (1967), who released 474 Microtus pennsylvanicus
into two inhabited 1-ha plots. In subsequent trapping the original residents were captured
repeatedly, but only 31 of the introduced voles were ever captured and only five (four females
and one immature male) were classified as having established themselves (i.e., were recaptured
on the grids where they had been released when trapping was resumed 3 weeks later).
Direct observations support the prediction that settlers and transients have difficulty penetrating
established groups (Andrzejewski et al., 1963; Armitage, 1984, 1986b; Eibl-Eibesfeldt, 1950;
Halpin, 1981; Hoogland, 1981; Lidicker, 1976; Metzgar, 1971, 1979; Reimer and Petras, 1967;
Rowe and Redfern, 1969). Settlers are unlikely to displace residents (Fitzgerald et al., 1981;
Jones, 1984), especially if settlers are less aggressive as suggested by Fairbairn (1978b) and Krebs
et al. (1978). If transients have been forced out of their natal or home range areas by aggressive
conspecifics they are likely to have been placed at a psychological disadvantage by the process.
Effects of defeat may be long lasting (Peters and Finch, 1961).
Residents are generally hostile toward strangers. Cox (1984) reported that Mus of both sexes
showed a preference for odors of their own group over those of an adjacent group. Young and
18 Rodent Dispersal
Stout (1986) found that food supplements increased the ratio of transient to resident Peromyscus
gossypinus on their study plot, but that the new arrivals were only briefly present and none
settled. Where encounters between resident Mus and introduced “immigrants” have been ob-
served, residents initiated agonistic interactions with the “immigrating” strangers (Hill, 1966).
In such encounters the initiating individual was usually the “victor” (Parmigiani et al., 1981;
Petrusewicz and Wilska, 1959). Andrzejewski et al. (1963) reported that mice that were added
to confined house mouse populations were attacked by residents, lost most fights, had low survival
probability, and were relegated to permanent subordinate status. Even with the use of an
“introducer” chamber that provided initial protection from attack, and with no opportunity for
egress, house mice of both sexes introduced into populations in large outdoor enclosures were
rarely able to penetrate established kin groups (Lidicker, 1976). Lidicker concluded that gene
flow would be largely the result of formation of new social units.
The probability that a transient will be able to establish itself within a population may be
determined largely by the degree of social stability and the extent of breeding activity within
that population. Baker (1981a) found that six of 10 female Mus introduced into high-turnover
populations in chicken barns established themselves and became pregnant. Myers (1974) reported
that of 11 house mice making spontaneous moves from one grid to another in a hayfield, six
remained at least 1 month. Most moves occurred prior to the start of breeding; none of the
individuals she released into her grids during the breeding season became established, but five
of seven released in the non-breeding season did so. Females may be more likely to be accepted
into social groups (Anderson, 1964; Baker, 1981la, 1981b), but this probably varies with species.
These results suggest that penetration of an established house mouse group might be more likely
if the would-be immigrant is female and arrives in the non-breeding season and if the social
structure of the target population is unstable. Although positive with respect to establishment,
unstable social structure and arrival in the non-breeding season could reduce the probability of
a gain in fitness.
Aggressiveness of residents toward unfamiliar individuals can vary with density. Wolff et al.
(1983) found that at high density, resident Peromyscus leucopus and P. maniculatus were
aggressive and behaviorally dominant (intra- and inter-specifically) on their home areas in 131
of 158 trials. When density was lower, using the same approach in the same area, Wolff (1985a)
found residents were not aggressive. The explanation of the contrasting results might be that
aggressiveness of residents declined as unoccupied areas became available; that transients or
settlers were “expected” to avoid contact when unoccupied space was readily available and thus
were not attacked; or that when transients were not able to find unoccupied spaces they turned
to challenging residents, thus inducing aggressive interactions.
Individuals that are accepted socially might still fail to breed or might breed only after a
considerable delay (DeFries and McClearn, 1970; Festa-Bianchet and King, 1984; Rowe and
Redfern, 1969; Singleton and Hay, 1983) during which they are subordinate and occupy marginal
parts of the habitat. Metzgar (1979) noted that individuals that were adult when initially en-
countered during a study of an unconfined population of Peromyscus maniculatus were likely
to breed only if few established residents were present. At other times newly established adults
tended to behave as “non-breeding subordinates.’ Schwartz and Armitage (1981) observed the
fates of 790 marmots (Marmota flaviventris) and found that only 40 succeeded in moving to a
new colony. Among these 40 settlers, only 15 appeared to have contributed genetically to their
new groups.
Reproductive success also could be limited if transients settle in poor habitat. Among herbivores,
individuals restricted to marginal areas might eat significantly higher quantities of toxic plant
species (Bergeron, 1980) and thus lower their survivorship or reproductive competence. Even if
not discriminated against by resident females, males that remain subordinate during a transitional
period may lack the capacity to activate females pheromonally (Lombardi and Vandenbergh,
1977).
Considering the vast literature on emigration, there are remarkably few data on immigration
Emigrant Fitness Hypothesis it's)
rates. Those available suggest that immigrants, as defined in Chapter I, make up a relatively
small proportion of most rodent populations. Berry and Jakobson (1974) observed replacement
of mates in house mice on Skokholm Island but did not calculate rates. Schwartz and Armitage
(1981) found that 5% of 790 marmots succeeded in moving to another colony and only 2%
reproduced. Foltz and Hoogland (1983) have estimated immigration rates as 10.4% for male
Cynomys ludovicianus and 2.8% for females. Bishop et al. (1977) reported that there was no
immigration into heavily poisoned Rattus norvegicus populations. Boonstra (1980) concluded
‘that at high density, microtine populations were almost closed to immigration. Turner and Iverson
(1973) speculated that young were wholly unable to establish home ranges in occupied habitat
during the period when litters were being produced. Hilborn and Krebs (1976), examining
movement between two grids less than 30 m apart, calculated that the proportion of disappearance
accounted for by immigration into a neighboring grid varied between 0.02 and 0.12% of emi-
grants. The proportion of disappearance accounted for by the appearance of marked individuals
in a removal plot 76.2 m distant averaged 11.8%. Immigration into an “unoccupied” habitat (a
removal plot) averaged twice that of immigration into the control grids. In striking disagreement
with this consensus, Holekamp (1986) reported that immigration was equal to emigration in two
populations of Spermophilus beldingi and Dueser et al. (1984) concluded that “immigration”
rates in populations of Microtus pennsylvanicus are very high.
I conclude that breeding is likely to be delayed whether a transient settles in occupied or
unoccupied habitat. The evidence suggests that immigrants are not likely to breed immediately
because resistance of residents to immigration opposes or delays breeding by new settlers. This
further discounts the argument that emigrants will mate sooner or more often than the philopatric
members of their cohorts.
Increased Fitness Through Emigration: Establishment in Better Habitat
Brown and Orians (1970) questioned whether lower fitness in poor quality habitat had been
adequately demonstrated. However, breeding success has been associated with preferred habitat
by Cockburn (1981), Cockburn and Lidicker (1983), Cockburn et al. (1981), and Spencer and
Cameron (1983). Diet quality, in particular, may be significant. Batzli (1986) showed that
Microtus californicus feeding on green vegetation produced more young than those on a less
favorable diet of grass seeds. Access to preferred diets would be most critical in periods of resource
shortage. At such times only the most favorably situated individuals would continue to reproduce
(Cockburn and Lidicker, 1983).
The supposition that emigration will result in acquisition of a site in habitat of better quality
is dubious. Gauthreaux (1978) argued that dominance was a means of regulating competition
and that dominance rank could be expressed in terms of the quality of the habitat occupied or
the distance to which an individual dispersed from its natal site. His argument assumes that
transients move to progressively less desirable habitat. Field observations support this view. Young
Clethrionomys born in poor habitat remained there and most young born in good habitat settled
in poorer habitat (Mazurkiewicz and Rajska, 1975). Lidicker (1985b) viewed favorable habitat
as islands surrounded by emigration sinks; he cited evidence that the highest quality habitats
are the ones most consistently occupied by Microtus californicus. Ostfeld (1985a) and Ostfeld
and Klosterman (1986) arrived at the same conclusion. Svendsen (1974) noted that marmots
classified as “avoiders’” on the basis of response to their mirror images lived peripherally to the
main colonies and were the least successful reproductively. It follows that highest quality habitats
are least available to settlers.
Adler et al. (1984) noted that Peromyscus leucopus found in marginal habitats are characterized
by smaller body size and lower recapture frequency. They assumed on this basis that individuals
found in such habitats had been emigrants. Krohne et al. (1984) described a sink area where P.
leucopus died out each winter. Among movements that Krohne et al. (1984) identified as “‘dis-
persal” (=emigration), 71% were into this sink. Four to nine times as many individuals moved
into the sink area as moved out of it. Merkt (1981) found that newly arrived P. maniculatus
20 Rodent Dispersal
settled in high quality habitat only when residents were experimentally removed. Van Horne
(1981) found that younger deer mice settled into habitat characterized by less proteinaceous
foods and low winter survival of mice. Sullivan (1979) observed bursts of movement of P.
maniculatus into clear-cut forest areas in late summer and fall. Winter survival was poor in
these areas compared with uncut forest. Bondrup-Nielsen and Karlsson (1985) characterized
movement of emigrant Clethrionomys as going from “optimal to low quality habitat.” Calhoun
(1963) and Metzgar (1971) found that under the conditions of their experiments transients settled
in less favorable locations or in the interstices between the territories of established residents.
Pokki (1981) observed that transient Microtus agrestis settled in wooded rather than in preferred
grassland habitat. Observing an unconfined population of arctic ground squirrels, Carl (1971)
reported that there was no overwinter survival in areas in which most transients settled.
Although Myers (1974) recorded movement of feral house mice from sparsely vegetated areas
to others that she judged to be more favorable, the general trend of the evidence is that dispersal
is rarely an upwardly mobile process in terms of habitat quality. Most emigrants might end their
lives in sink habitats (Anderson, 1970; Calhoun, 1962a, 1963; Lidicker, 1975; Tamarin et al.,
1984). Introductions into apparently suitable habitats not occupied by conspecifics often fail (e.g.,
Berry et al., 1982).
Even if an animal mates while transient it is unlikely to have gained in fitness through
emigration if young are produced in inferior habitats as a result of matings with other transients,
or matings with residents of poor quality habitat that are stressed by nutritional deficiencies,
exposure, and social discrimination. Emigration is an unlikely road to increased fitness through
increased habitat quality.
Increased Fitness Through Emigration: Emigrant Advantage Through Heterotic Mating
As Lidicker (1962) suggested, an emigrant that succeeds in mating will probably share fewer
common ancestors with its mate than will a non-emigrant. Outcrosses of laboratory mice (Mus
musculus) from previously inbred lines give rise to larger litters of more vigorous offspring (Chai,
1959; Green, 1966; Lynch, 1977). Hybrid vigor acquired in this way could also carry over to
females of the following generation (Lynch, 1977).
A vital point that is often overlooked is that heterosis is likely to be proportional to the degree
to which it has been preceded by inbreeding. It will be most evident when considerable inbreeding
has occurred in the past (Green, 1966). In an ideally panmictic population the average outbred
mating would not increase heterozygosity. In other words, the potential gain in fitness as a result
of heterosis is greatest where there has been a tradition of incestuous mating (parent-offspring,
sibling) or close inbreeding (cousin, half-sibling).
Shields (1982) has emphasized that outbreeding entails genetic costs that oppose the possible
heterotic gains. Fitness of offspring resulting from outbred matings may depend on whether
adaptive combinations of genes and alleles have been disorganized (Selander et al., 1969a; Shields,
1982). Pre-existing combinations would have been pruned by selection so as to be adaptive.
Where this is the case, novel combinations resulting from outbreeding are equivalent to mutations
insofar as they have a high probability of being disadvantageous. The chances of lower fitness
might be slight if an emigrant settles near the natal site, but should increase with dispersal
distance and/or difference in habitat.
There is little information on the question of heterosis as a result of outcrossing in natural
populations. In a recent experiment in which incrosses and outcrosses of house mice from discrete
commensal populations occupying small granaries were compared (Anderson, unpublished),
outcrosses led to significant increases in mean litter size at birth. However, Martell (1983) found
no differences in litter size of Peromyscus maniculatus in newly colonized clear-cuts and un-
disturbed forest. Juvenile persistence (survival?) was low in newly colonized areas. Demonstration
of heterosis at a single locus has proved elusive in natural animal populations except in the case
of sickle-cell anemia in man. The sickle-cell case illustrates the point that the adaptiveness of
new allelic combinations depends on their appropriateness to the habitat (heterosis at the sickle-
Emigrant Fitness Hypothesis 21
cell locus is adaptive only where malaria is present). Outbreeding as a result of emigration may
therefore produce allelic combinations which are less adaptive to the habitat than are the parental
combinations.
It could be significant in this context that in some populations there appears to be a strong
tendency to associate with close relatives. King (1983) reported that only five of 104 Peromyscus
born on his study site and remaining until 37-40 days of age were ever found in the company
of a non-relative.
Further experiments are needed to determine if the litter-size heterosis observed in outcrosses
of house mice from granary populations can be generalized to other species and habitats. Even
where such benefits occur, increased fitness is not a necessary outcome because the adaptiveness
of larger litter size at birth, like that of larger clutch size in birds (Lack, 1966), will depend on
parental ability to provide the necessary nourishment.
The evidence indicates that heterotic gains are possible if there has been previous inbreeding,
but that if heterotic gains do occur in nature they could be negated or neutralized by the
phenotypic inferiority of immigrant parents, inferior quality of the habitat into which the parents
have immigrated, and low status within the new social group.
Increased Fitness Through Emigration: Avoidance of Inbreeding Depression
Some inbreeding occurs in all finite populations. Any consequent reduction in number and
viability of young is the reciprocal of heterotic gain. Inbreeding can be deleterious in two ways.
It can eliminate any advantage due to heterozygosity, and it can increase the probability that
unconditionally deleterious or lethal alleles will occur in the homozygous condition. The prob-
ability that recessive alleles will be homozygous increases with the proportion of parental alleles
shared by potential mates.
For clarity it is important to keep in mind that inbreeding may occur in the context of a
family (parent-offspring, sibling, or half-sibling matings, to which the terms “strong inbreeding”
or incest can be applied) or because a species is structured in such a way that deme size is small
and matings with cousins, uncles, aunts, nieces, or nephews (close inbreeding) are highly probable.
Although the basic problem of shared ancestral alleles is identical in both strong and close
inbreeding, the social and behavioral contexts are distinct. The arguments that avoidance of
inbreeding would favor evolution of emigratory tendency have been based largely on the potential
genetic consequences of incestuous matings (strong inbreeding).
Avoidance of inbreeding depression has appeared to be one of the stronger and more popular
arguments for the EFH. Murray and Smith (1983), for example, wrote that “kin-mating aversion
may function to promote migration in most mammalian species.” Sherman and Holmes (1985)
advanced inbreeding avoidance as the major adaptive force behind kin recognition. Because of
the apparent strength of the inbreeding avoidance argument, and because the question has a
major bearing on the alternative to the EFH that I propose, a detailed discussion of the evidence
on the cost of inbreeding is appropriate.
As pointed out by May (1979) and Moore and Ali (1984), extrapolation from the evidence
that forced inbreeding in the laboratory or in other captive situations reduces litter size or
viability of young might have led to fabrication of elaborate hypothetical constructs with in-
adequate foundations. Attempts at a more balanced view (e.g., Bateson, 1983; Bengtsson, 1978;
Partridge, 1983; Shields, 1982) have only recently surfaced. These efforts make it clear that the
net cost or benefit is dependent on the context in which inbreeding occurs.
The hypothesis that emigration would increase fitness by avoiding the potential cost of mating
with a close relative rests on three assumptions. The first is that there will be a net loss of fitness
in a mating with a relative. The second is that there is a net gain in fitness through avoidance
of inbreeding by means of emigration. The third is that the potential for inbreeding is great
enough so that there is a need to emigrate to avoid the net cost, if any.
The theoretical basis for inbreeding cost is straightforward. All individuals carry recessive
alleles that are deleterious in the homozygous condition. The more closely potential mates are
22 Rodent Dispersal
related to each other, the more likely it is that two alleles at any given locus will have been
derived from the same ancestral allele and the greater the probability that any deleterious
recessives present will appear as homozygotes. Much concern has been expressed with regard to
costs of inbreeding in small populations of endangered vertebrates in the wild and in captivity.
A summary of the results of inbreeding of large mammals in zoological parks (Ralls et al., 1979)
showed that with inbreeding coefficients of 0.25 or greater the number of surviving young was
lower for the majority of species than when matings took place between less closely related
individuals. It is important to note, however, that this was not evident in all species studied.
With respect to rodents, specifically, the evidence for inbreeding cost is inconclusive. Con-
sequences of incestuous matings in rodents have been examined in Peromyscus maniculatus
(Haigh, 1983q; Hill, 1974) and in more detail for both laboratory and wild stocks of Mus musculus
(Chai, 1959; Connor and Belluci, 1979; Falconer, 1960a, 1960b; Lynch, 1977; McCarthy, 1965,
1967; Roberts, 1981; Wallace, 1981).
Early work with laboratory stocks of Mus musculus compared performance of outcrosses
with that of inbred stocks from which the parents were derived. Chai (1959) found that outcrosses
between inbred strains tended to have lower mortality in early life and longer mean life spans
than the inbred parent strains. Falconer (1960a) began inbreeding with an outbred stock derived
by crossing two unrelated inbred laboratory lines. Average litter size in 30 lines maintained
through full sib matings dropped by 0.49 young per 10% increase in the inbreeding coefficient;
in 20 lines initiated with a double first cousin mating followed by full sib matings mean litter
size dropped by 0.56 young per 10% increase. Losses in the second experiment were partitioned
as 40% due to lowered maternal fertility and 60% due to reduced viability of the young.
Connor and Belluci (1979) found that although only five of 10 inbred house mouse lines
survived 20 generations of inbreeding, litter size decline occurred primarily in the five lines that
became extinct. In all 10 lines, survival of young in early life showed an increase up to the 0.50
level. At the end of 20 generations only one of the five surviving lines showed the anticipated
degree of homozygosity. In the same series of experiments, stocks held at eight breeding pairs
and thus subject to moderate inbreeding failed to show any reduction in fertility.
Because the initial stocks used by Chai (1959), Connor and Belluci (1979), and Falconer (1960a)
were inbred laboratory lines, each should theoretically have been purged of deleterious lethals.
If this was indeed the case the data must reflect loss of heterosis, rather than expression of recessive
lethal homozygotes.
Even where inbreeding does reduce the number of first generation offspring, the consequences
may be somewhat ephemeral. An important point with respect to Falconer’s (1960a) work is
that only half of the inbred lines showed depression in litter size. Lines showing depression died
out within a few generations, whereas those not showing depression continued to produce litters
as large as those expected under random mating (Falconer, 1960a). If lineages carrying deleterious
recessives are eliminated almost immediately, even under laboratory conditions, surviving de-
scendants of inbred matings could benefit sufficiently from their lack of the deleterious alleles
to compensate for any initial loss in fitness suffered by the original parental pair.
Use of wild stocks of house mice in studies of strong inbreeding has provided interesting results.
Like Connor and Belluci (1979), Wallace (1981) and Lynch (1977) found that inbreeding failed
to produce the anticipated reproductive depression. Lynch suggested that wild stocks from which
her lines were started were partially inbred so that her initial crosses (with mice collected at
random from several farms) were heterotic and that heterotic maternal effects extended to the
second generation. Wallace (1981) found that her wild stocks maintained mean litter size at 5.5
young through five generations of sib mating despite a 60% loss of heterozygosity. There was
no appreciable reduction in fitness as measured by proportion of fertile females or mortality
between birth and 15 days of age.
Under laboratory conditions, inbreeding of house mice taken from wild stocks that were
presumed to be outbred thus failed to produce the amount of inbreeding depression that Falconer’s
(1960a) calculations would lead one to expect. This appears to imply two seemingly contradictory
Emigrant Fitness Hypothesis WD
conclusions: first, that the store of heterozygosity is sufficiently high so that reduction through
five generations of incestuous matings does not reduce litter sizes as it apparently did in Falconer’s
study; second, that there is sufficient inbreeding in natural house mouse populations so that
further inbreeding is of little or no consequence because most deleterious alleles and/or lineages
carrying them have already been eliminated. In any case it seems evident that in wild stocks of
house mice even strong inbreeding is not as costly as basic theory would imply.
Several arguments give some support to the idea of resistance to inbreeding depression in litter
size. Unlike the ungulates studied by Ralls et al. (1979), many rodents produce large numbers
of ova at each estrus. When larger numbers of eggs are ovulated than can be accommodated as
zygotes implanting in the uterus, early losses would reduce intrauterine competition and com-
pensation for pre-implantation losses might be possible. The reduced production of young in
Falconer’s inbred lines was not due to ovulation of fewer eggs; most loss of zygotes occurred
prior to implantation (Falconer and Roberts, 1960) in contrast to other studies reporting more
post-implantation loss. For example, in inbred lines McCarthy (1965) demonstrated significant
early post-implantation losses and Hollander and Strong (1950) found average mortality was
15%, mostly in the first 3 days post-implantation. Bowman and Roberts (1958) reported a
correlation between the number of eggs ovulated and the amount of intrauterine loss, but were
unable to demonstrate correlation between loss and number of implantation sites. Although the
evidence is ambiguous, the possibility of compensatory intrauterine survival should not be re-
jected.
Postnatally, reduction of sibling competition might compensate further for any inbreeding
depression. Dapson (1979) found that although female Peromyscus with large litters weaned
more young, the percent of young weaned was higher in smaller litters. Fuchs (1982) reported
that in addition to higher survival, smaller litters were characterized by higher individual growth
rates.
Some evidence from studies of other wild rodents also suggests that inbreeding depression
could be less significant than is generally assumed. Lidicker (1979) reported normal litter sizes
in confined populations of Microtus californicus that had been initiated with a single pair of
adults. Although Hill (1974) reported that sibling Peromyscus pairs delayed first reproduction
and had lower lifetime reproduction than did non-sibling pairs, Haigh (1983a) found that father-
daughter matings did not differ from matings of the daughter with an unrelated male in the
proportion of females that conceived, age of the female at first reproduction, size of litters, total
number of litters, or total number of young produced. Weights of offspring at 2 days of age and
survival of offspring to 21 days were less in incestuous matings, but the difference was slight.
Outbreeding creates a large effective population size (N.). Deleterious mutations can accu-
mulate in large panmictic units as a consequence of relaxed selection. As Moore and Ali (1984)
emphasized, discussions of inbreeding depression often overlook the fact that inbreeding depres-
sion will only occur in populations that have had opportunities to accumulate deleterious mu-
tations. If N. is small, deleterious mutations could decline in frequency (or be eliminated) as a
result of drift or selection against homozygotes, or both (Lewontin, 1962). Effective population
size is unknown for most rodent populations and there is inadequate justification for the common
belief that it is large. Selection pressures in rodents have yet to be extensively documented
(Gaines, 1981, 1985). Therefore, neither large population size nor relaxed selection can be
assumed.
Any net cost of inbreeding must be balanced against the cost of emigrating to avoid inbreeding.
I suspect that inbreeding cost is relatively stable, but the cost of emigrating might be more
variable as seasons and population densities change. Cost-benefit relationships have been explored
in some detail in the models of Waser et al. (1986). The models predict that even in monogamous
species such as Microtus ochrogaster it is the cost of inbreeding avoidance (rather than the cost
of inbreeding) that will determine whether there will be selection against inbreeding. The models
also suggest that inbreeding depression will generally be less costly than mortality during tran-
siency, especially where mating systems are polygynous and a male forfeits few outbred matings
24 Rodent Dispersal
by mating with an offspring, but forfeits many opportunities for incestuous matings if he behaves
so as to avoid inbreeding. This seems to imply that where females are strongly philopatric and
both male and female ranges are stable, a male should not refrain from inbred matings. The
models indicate that inbreeding by males is favored under a wider range of conditions than is
the case for females.
An earlier set of modeling studies led Bengtsson (1978) to conclude that where the inbreeding
coefficient equaled 0.25, inbreeding would be favored if more than 40% of males produced died
as emigrants. He regarded this as an improbably high loss but for populations of small rodents
it is probably unusually low. Evidence for low success of emigrant marmots has been cited above
(Schwartz and Armitage, 1981). Similarly, success of emigrant male Spermophilus parryii appears
to be on the order of 15% (McLean, 1982). L. Getz (pers. comm.) has observed success of
emigrants to be in the 25-32% range in Microtus ochrogaster. Bengtsson (1978) calculated that
a strategy that increased inbreeding by 1% would be favored if it simultaneously reduced mortality
by 3%. He concluded that if a population had been inbreeding for a long time, eliminating
deleterious mutants through selection, no significant gain in fitness would accrue from outcrossing.
May (1979) reviewed Bengtsson’s model and emphasized that the decision to emigrate or to
inbreed must be viewed in a cost-benefit context and pointed to the need for more information
on the kinship structure and actual costs of inbreeding in natural populations before inbreeding
avoidance is used as a basis for explaining behavioral phenomena.
The models discussed above deal primarily with outbreeding costs in terms of risk of death
or failure to reproduce. Another cost has been proposed by Shields (1982). He argued that because
most genetic changes can be considered either individual or familial lethals, and favorable alleles
and combinations can be shared by members of a family but are unlikely to be shared with
members of other families, extrafamilial matings might have an average reduction in fertility
(as much as 100% in the case of karyotypic mutations, and as little as 5% or less in the case of
point changes).
Shields (1982) proposed that when a point mutation creates a favorable epistatic relationship
in the local habitat, maintenance of the coadaptive combination will be favored through intra-
familial mating. He argued that the traditional view that inbreeding is disadvantageous stems
primarily from consideration of intralocus effects, and reasoned that there will be an optimal
level of inbreeding for each species, based on the relative predominance of positive epistasis or
inter-locus factors in adaptation. He concluded that while an optimal level of inbreeding would
rarely include incest, it might involve close inbreeding within demes in which N, was under
1,000 individuals.
The third point raised near the beginning of this section was whether the opportunity for
inbreeding was sufficient for the evolution of mechanisms that function to prevent it. High
inbreeding coefficients require that breeding structure be stable over several generations. For
most populations, environments are so variable and the existence of individuals, families, and
lineages so transitory, that there might be little opportunity for inbreeding and thus little selection
for inbreeding avoidance. Even in long-lived rodents such as marmots the life span of lineages
may be so short that any increase in homozygosity due to inbreeding is reversed by subsequent
outbreeding (Armitage, 1984). As Greenwood (1983) has said, avoidance of inbreeding as seen
in nature is perhaps as likely to be an unselected effect as it is a cause of dispersal.
The best case for emigratory behavior that effectively reduces inbreeding can be made in
those ground squirrels in which reproductively successful males shift burrow sites between
breeding seasons (Michener, 1980; Sherman, 1981) or in which juvenile males emigrate before
their first hibernation (Sherman, 1981). Even here it is perhaps too easy to conclude, as has
Holekamp (1984), that the data on emigration and immigration are consistent with the hypothesis
that dispersal evolved because it could “function to minimize incest.” Moore and Ali (1984) gave
detailed consideration to the question of whether emigration generally accomplishes this and
felt that it did not. They argued that sex differences in emigratory tendency could have evolved
on the basis of inbreeding depression only in a group selection context, and emphasized (p. 95)
that “since inbred siblings are more closely related than outbred ones, and hence more able to
Emigrant Fitness Hypothesis 25
benefit from kin selection, inbreeding can be seen as a potentially beneficial phenomenon that
promotes increased altruism and sociality.’ Their conclusion was that although inbreeding is not
inherently maladaptive, emigration (usually necessary for outbreeding) probably is, with the
result that philopatry and consequent inbreeding should generally be favored. In their view the
evidence available from studies of both birds and mammals failed to support the belief that a
male/female differential in probability of emigration could be explained on the basis of inbreeding
avoidance. They also reasoned that if the mean dispersal distance were nearly equal for the two
sexes, dispersal would have little effect on inbreeding.
If emigratory tendency has evolved because of its increment to fitness through inbreeding
avoidance, I would expect the sex that has the most to lose through inbreeding to be the one
with the highest emigratory tendency. In polygynous species, females seem more likely than
their brothers to suffer from inbreeding depression (through proportionately higher loss of re-
productive potential), yet male rodents are the emigration-prone sex. In polygynous species
where males make little or no post-copulatory investment in offspring and do not sacrifice
additional matings, males have little to lose through inbreeding (Smith, 1979). As would be
predicted, kin recognition appears to be least developed in males, but it is difficult to argue that
the sex with the least to lose through inbreeding should be the one most likely to emigrate.
There is one further argument against the importance of inbreeding avoidance that should
be mentioned. Resident rodents resist immigration. If inbreeding is to be avoided and outbreeding
is advantageous, then this resistance is surprising.
Summing up, inbreeding in natural populations of rodents may not be inevitably costly, may
be less costly than has been conventionally assumed, or may be advantageous. Reduced litter
size could be compensated for by reduced sibling competition, and inbreeding could speed
elimination or oppose accumulation of deleterious alleles. Provided that an inbred mating does
not occur at the cost of an opportunity for an outbred mating, any residual costs must be balanced
against loss of inclusive fitness through disappearance, mortality, and/or reduced success of
emigrant relatives as compared with non-emigrants, or through disruption of co-adapted gene
combinations (Bateson, 1983; Partridge, 1983; Smith, 1979). The tendency to view the laboratory
evidence on inbreeding depression as prima facie evidence that inbreeding will be avoided in
nature is not justified. It is difficult to reconcile the observation that in mammals the female sex,
which has the most to lose through inbreeding depression, is the least likely to emigrate. Avoidance
of inbreeding is not an automatic, or even probable, source of emigrant fitness.
Increased Fitness Through Emigration: Avoidance of Population Crashes
Lidicker (1962:29) suggested that emigrants should benefit if they were able to “avoid getting
involved in devastating population crashes (whatever their cause) by moving out of potentially
congested places.” There is little evidence to show that a “population crash” as such should have
an adverse effect on individual survival or reproduction, and it is not intuitively obvious that
emigrating from a habitat occupied by a declining population should increase individual fitness
as long as food, cover, and mates are available. As crude density declines, per capita resource
availability should increase, and exposure to contagious disease or stress resulting from social
pressure or resource depletion would presumably be reduced. Because site-tenacious or philopatric
survivors could benefit as a result of reduced competition in such a situation it is difficult to see
how “avoidance of a crash” could select for an emigratory tendency.
Observational evidence suggests that the number (and presumably the proportion?) of indi-
viduals emigrating tends to decline in declining populations (e.g., Gaines et al., 1979b). For
emigration to function as a means by which individuals avoid population crashes, emigrants
would have to possess a means of sensing the impending crash (response to crowding?) and leave
before the decline took place. Mass emigration at this time should, however, serve to reduce the
chance of a catastrophic decline, making the reasoning somewhat self-defeating. Most evidence
shows that the survivors of sudden declines are in the optimal habitats, not in marginal habitats
as Lidicker (1962) imagined.
An alternative argument might be that groups in which young inherited a tendency to emigrate
26 Rodent Dispersal
would be less likely to suffer “overpopulation” and therefore be less susceptible to “crashes.”
However, the departure of emigration-prone genotypes would strip the groups of the relevant
alleles, destroying the supposed group advantage in the process.
The Evidence for Emigration-Prone Genotypes
The EFH is, at the very least, strongly linked to the concept of genetic variation in innate
emigratory tendency. As Lidicker put it, the EFH “requires that emigratory tendencies can
indeed be controlled genetically” (Lidicker, 1962:30). Inherited variation in tendency to emigrate
seems to me to be essential to the “innate disperser” concept proposed by Howard (1960) and
the “pre-saturation” concept proposed by Lidicker (1975, 1985a). Although some may not accept
the argument that the hypothesis is totally dependent on the existence of alleles programming
emigration, the importance of the issue cannot be denied.
The initial suggestion that such innate programming existed in rodents (Howard, 1960) was
based on data on the distribution of dispersal distances. Available distribution data are leptokurtic.
As Murray (1967) argued, and Waser (1985) has demonstrated with a model, a leptokurtic
distribution of dispersal distances can be explained without a requirement for a specific poly-
morphism for emigratory tendency.
In many invertebrate populations, specialized forms or life history stages equipped morpho-
logically or behaviorally, or both, for long distance movement are well known. However, no
studies have convincingly demonstrated parallel polymorphism in rodents despite numerous
attempts to demonstrate correlations between biochemical phenotypes and tendency to emigrate.
These efforts to correlate such phenotypes with emigration have either failed to show any
correlation (Berry and Jakobson, 1974; Blackwell and Ramsey, 1972; Gaines and Krebs, 1971;
Gaines et al., 1979b; Krohne et al., 1984; Myers, 1974; Schwartz and Armitage, 1981; Singleton,
1983) or have relied on designs that are suspect because they did not unambiguously distinguish
non-emigrant and emigrant categories, or because they did not specify the source of the emigrants.
I think it worthwhile to review these technical weaknesses in some detail.
The majority of such studies categorized individuals captured on removal plots as emigrants
(commonly referred to as “‘dispersers’’), and compared this sample with the original residents,
or with animals resident on a “control” area somewhere in the vicinity (Baird and Birney, 1982a;
Fairbairn, 1978a; Gaines and Johnson, 1982; Hilborn, 1975; Keith and Tamarin, 1981; Krebs et
al., 1976; Massey and Joule, 1981; Myers and Krebs, 1971; Pickering et al., 1974; Stafford and
Stout, 1983; Tamarin, 1977a). As discussed earlier, removal plots appear to draw on a pool of
unestablished animals. These may be diverse in microgeographic origin (Baird and Birney, 1982a,
1982b; Desy and Thompson, 1983; Dueser et al., 1981; Krebs et al., 1976, 1978; Schroder and
Rosenzweig, 1975; Small and Verts, 1983; Williams and Cameron, 1984). Typically, only a small
proportion originate on any nearby “control” area. For example, Krebs et al. (1976) reported
that only 15% of the animals captured on their removal plot came from the nearby control. The
fraction of removal grid settlers known to originate on the control plot appears to have been
approximately the same in the study of Myers and Krebs (1971). Stafford and Stout (1983) noted
that only 11 of 88 Sigmodon captured on two removal grids came from nearby control grids.
Mihok et al. (1985b) trapped a “depleted” grid for 78 marked Microtus that disappeared from
a nearby 3.24-ha control grid. Among 106 animals captured they found only one of the marked
voles. In another investigation, Mihok et al. (1985a) concluded that Clethrionomys appearing
on a removal grid had come from an “inexhaustible” pool over a large surrounding area. Taken
together, these observations support speculation that the majority of individuals captured on
removal grids come from considerable distances (Boutin et al., 1985).
With a few possible exceptions (e.g., Foltz, 1981b; Foltz and Hoogland, 1983; Keith and
Tamarin, 1981), rodent populations show temporal and/or microgeographic genetic variation in
allelic frequencies (Anderson, 1964; Berry, 1963; Berry and Jakobson, 1975; Bowen, 1982; Chesser,
1983; Dunn et al., 1960; Gaines et al., 1978; Jannett, 1981b; Kawata, 1985a; Krohne et al., 1984;
Massey and Joule, 1981; Myers and Krebs, 1971; Patton and Feder, 1981; Schwartz and Armitage,
Emigrant Fitness Hypothesis 27
1981; Selander, 1970a, 1970b, 1976; Semeonoff and Robertson, 1968; Singleton, 1983; Smith et
al., 1978). If the vast majority (80 to 90%) of animals captured on removal plots are of unknown
spatial and temporal origins, differences between total removal plot samples and any specific
resident (“control plot”) sample in allelic and heterozygote frequencies are to be expected on
the basis of microgeographic variation alone. It is this uncertainty with regard to the origin of
removal samples in space and time that invalidates the majority of resident /emigrant comparisons,
because only those transients and settlers known to have originated on the control area can
legitimately be used in a comparison of emigrant and philopatric members of the control
‘ population.
Most studies have also failed to take into account the reports that frequencies of biochemical
variants could change seasonally due to shifts in selection pressure (e.g., Berry and Murphy,
1970; Fedyk and Gebczynski, 1980). If such variation occurs, comparison of sedentary (or
philopatric) and emigrant animals must also be restricted to members of the same seasonal cohort.
Studies reporting correlation between emigratory tendency and biochemical phenotype have not
met this criterion.
Because it is frequently cited in support of the view that emigrants are genetically different
from non-emigrants, I have chosen the study of Myers and Krebs (1971) to illustrate the mis-
interpretations risked in the removal-grid approach. The conclusion of this study (based on
comparison of the transient-settler sample on the removal area with that from the nearby controls)
was that ““Tf-E and Lap-S phenotypes were more common among dispersing animals” (Myers
and Krebs, 1971:53). This was interpreted as indicating a possible association between the un-
derlying genotypes and tendency to leave the control area, or equivalent areas with similar gene
pools. Fortunately, the data presented by Myers and Krebs (1971) allow comparison of frequency
of these alleles on the control grids (I and F) with the sample of animals actually known to have
moved from grid I to the removal grid K. Data were presented for six seasonal samples for each
of these alleles in Microtus pennsylvanicus. In only two of the six samples of males was Tf-E
more common in those known to have moved from Grids I and F than in the control sample
(residents on grids I and F). Tf-E was also more frequent in only two of six samples of females
known to have moved from grids I and F to grid K. In only one of the six samples was the
frequency of Lap-S higher in animals known to have moved from grids I and F to grid K (Krebs
and Myers, 1971: tables 10, 11, 12; pp. 66-68). Therefore the valid comparison (emigrants vs
residents from the same source) shows a trend just the opposite of that reported by Myers and
Krebs (1971) in 183 of 18 comparisons.
Removal techniques recently have been criticized on still other fundamental grounds (Dobson,
1981; Krohne et al., 1984). I believe the evidence for genetic differences between emigrant and
philopatric individuals based on removal studies done to date cannot be accepted. Alternative
approaches to demonstration of inherent migratory tendency taken by Beacham (1979b), Hilborn
(1975), and Garten (1976) are equally open to criticism, failing either to satisfactorily discriminate
comparable emigrant and non-emigrant groups, or to eliminate other sampling, maternal, or
environmental factors that could account for the differences observed.
As Gaines and McClenaghan (1980) pointed out, failure to find a correlation between elec-
tromorphs and tendency to emigrate does not prove that there are no alleles programming an
emigratory tendency. The chance of finding a correlation between any particular electromorph
and such a complex behavior is indeed quite small. If the EFH in general and the specific
“innate” and “pre-saturation” hypotheses proposed by Howard (1960) and Lidicker (1975)
require such polymorphism, the failure of the numerous attempts to demonstrate polymorphism
weakens the credibility of the EFH, but does not disprove it.
Rejection of the EFH?
The EFH has never been explicitly explored in detail. It would be good if some adherent
would do this. How does the EFH account for maternal nepotism toward daughters, for the
greater tendency of daughters to philopatry, or for the tendency of male dispersal distances to
28 Rodent Dispersal
exceed female dispersal distances? What behavioral predictions can be based on the EFH and
are they supported by the available information?
To date, the EFH has been accepted almost casually. Its essential core is that emigratory
tendencies have evolved because emigrants gain fitness relative to non-emigrants. There have
been no direct and systematic tests of this assumption, although Jones (1986) has shown that
philopatric Dipodomys spectabilis survive better than even those members of their cohorts that
do succeed in settling elsewhere. I think it is fair to state that the main support for the core
concept of the EFH has been the reasoning that because animals emigrate, the assumptions of
an average net gain in fitness to emigrants and the existence of polymorphism for emigratory
tendency must be correct. In this superficial acceptance of the EFH, the costs of emigration and
establishment at a new site have been ignored (Dobson, 1982). The preceding review indicates
that, contrary to the reasoning above, emigrants are unlikely to gain fitness, and the adaptiveness
of emigration for emigrants, even in the best possible light, is uncertain (Festa-Bianchet and
King, 1984). There is good reason to conclude, as did Moore and Ali (1984), that emigration is
maladaptive for emigrants, most of which find their way into emigration sinks.
The suggestions that emigration has evolved because individuals that emigrate have a higher
probability of surviving and reproducing, are likely to occupy better habitat, produce larger
litters, or otherwise accrue higher fitness than conspecifics that do not emigrate have been shown
to be poorly supported. Although it is possible that emigrants may avoid costs of inbreeding
depression through matings with near relatives, or gain fitness through matings that produce
heterotic offspring, these gains are not certain and are likely to be exceeded by the costs of
emigration, transiency, and immigration. As it stands, I feel that the EFH is a poorly supported
hypothesis. It should be be rejected if a better one can be developed. This is not to say that
emigration is never the best or the only available strategy. It does suggest that the phenomena
encompassed by the term dispersal are unlikely to have evolved on the basis of benefits to
emigrants.
Il
THE RESIDENT FITNESS HYPOTHESIS
The dispersal hypothesis presented in this chapter rests on the propositions that emigration
arises from an interaction between dominants and subordinates, that parents are dominant to
their offspring, and that the behavioral processes evolved on the basis of parental benefit.
Among others, Beacham (1979b), Christian (1970), Gauthreaux (1978), and Krebs (1978b)
have concluded that behavioral_interaction-between_dominant and subordinate individuals is
likely to be the proximal cause of emigration. Established residents are generally dominant over
other categories of individuals. Parents are established and young are not, and it is in parental
interest to control the distribution of propagules (Comins et al., 1980; Hamilton and May, 1977;
Horn, 1983). Fitness is dependent not only on the number of offspring born and reared, but also
on the amount of competition between parents and their maturing young, and on the spatial
distribution of those offspring that reproduce. Disbursement of young is thus an important aspect
of parental strategy. If, as Alexander (1974:340) stated, “the entire parent-offspring interaction
evolved because it benefited one of two individuals—the parent,” it follows that dispersal has
evolved on the basis of the fitness of resident parents, and that parents behave so as to achieve
an optimal allocation of offspring to philopatry or emigration. This approach expands, and
examines with specific reference to rodents, the suggestion of Hamilton and May (1977) that
parental manipulation might play a role in the evolution of dispersal systems.
The focus of this Resident Fitness Hypothesis (RFH) can be brought out clearly by an analogy.
Operationally, breeding rodents can be as sedentary as plants. Like plants, therefore, their fitness
is strongly influenced by the dispersal of their offspring. Like plants also, they can face competition
from offspring that establish at the natal site. Angiosperm “young” (embryos) are non-motile.
Plant propagules are distributed by means of adult adaptations (Howe and Smallwood, 1982);
well-known examples include the height and position of seed-bearing structures, and the coatings
of parental tissue that may be wing-like, hooked, sticky, nutritious, or attractive. Adult plants
also have defenses (such as shading, root competition, and allelopathy) that restrict competitive
establishment of their propagules (philopatry) or those of other conspecifics (immigration). An-
giosperm dispersal is a matter of parental adaptation and can be analyzed in terms of parental
strategies that cope with both competitive parent-young interactions and optimization of the
balance between inbreeding and outbreeding (Levin, 1981; Price and Waser, 1979). The RFH
proposes that emigration of young rodents similarly is based on adult adaptations, and that
mobility of rodent young is exploited by established residents to control philopatry and emigration
and to block immigration of less related individuals. Exploration of these ideas as to how residents
behave and offspring might respond requires consideration of inclusive fitness (Hamilton, 1964a,
1964b) and parent-offspring conflict (Trivers, 1974).
The players in the dispersal game are residents and potential residents. The latter consist of
offspring of the residents (closely related potential recruits) and transients (more or less distantly
related potential recruits). The resident role with respect to transients is relatively simple. Tran-
sients are competitors, distantly related at best, and rarely to be tolerated even as potential mates.
The parent-offspring relationship is much more complex and dynamic. Initially, offspring are
the currency of classical fitness. As offspring mature, parent-offspring conflict over emigration
is inherent (Horn, 1983). Maturing offspring can become both competitors and potential mates,
yet they remain relatives with whom we should expect interactions to be governed by the rules
of inclusive fitness. Parents can be expected to behave so as to further the survival and reproduction
of their offspring, but must also behave so as to minimize competition that jeopardizes parental
29
30 Rodent Dispersal
reproduction, competition that threatens survival of and reproduction by their own siblings, and
competition among young that threatens survival or reproduction of their own offspring. Parents
and offspring of the opposite sex can offer each other matings in which a higher proportion of
the alleles transmitted to the subsequent generation are identical by descent. It may be advan-
tageous to parents, in order to minimize competition, to force offspring to emigrate, despite the
heavy odds against successful establishment elsewhere. Wide distribution of the genetic contri-
bution of the offspring may, in itself, be important enough to parents to justify the cost of lowered
offspring fitness, but offspring may gain most by avoiding the cost of emigration and settling on
the natal site. However, this conflict is not a static state. Optimal strategies for both parents and
offspring shift with the resource supply, the residual reproductive value of the parents, and the
period of seasonal breeding available to offspring. This dynamism is especially acute in species
in which females are polyestrous, and maximum life span encompasses a single annual cycle.
As parental investment can be expected to vary with expectation of future survival and repro-
duction (Clutton-Brock, 1984; Morris, 1982), parental behaviors and offspring response will be
specific to successive litters as the breeding season progresses.
The immediate goals at stake in the dispersal game are resources that are “fixed” in space.
These resources, to which home range and social position are the keys, are sex-specific. Resident
males can compete for females; females can compete for nutritional resources, for sites in which
to rear young, or for such paternal investment as the mating system makes available. These
resources, however, are merely means toward the ultimate goal of both parents and offspring:
relative representation of alleles, identical by descent with those they carry, in the gene pool of
the future. Resident parents are constrained in their treatment of offspring by the fact that the
offspring represent their primary genetic contribution and are also relatives through whose
welfare there may be parental benefit. Offspring are constrained by the relatedness of their
parents.
Because offspring compete in different ways and share different sets of alleles with male and
female parents they relate to each parent differently. Offspring fitness is also influenced differently
by siblings of the same and of the opposite sex. As offspring approach maturity their requirements
and those of their parents increasingly coincide. In order to breed, an offspring might require
a home range of its own (philopatric or not), but it might also benefit through helping its parents
to rear further young. The least expensive way to obtain a home range, from the point of view
of offspring, is to settle on the natal range. A home range encompassing all or part of the parental
range could become available to one or more offspring through parental death, parental emi-
gration, or nepotism. Forceful takeover of the parental range by an offspring is unlikely. Parental
cooperation or the death of the parent is required. Parental cooperation (nepotism) can only be
expected when the parent will gain more through use of that range by an offspring than by
using the range itself (e.g., when parental reproductive value is so low that the offspring can
contribute more to the parent’s fitness than the parent can).
Small size and inferior social status limit the options open to offspring. Offspring could emigrate
when given no other choice, minimize or avoid competition by delayed growth and/or maturity,
or contribute sufficiently to parental reproduction to compensate for the competitive cost of
continued offspring presence.
The crux of the RFH is that residents control the game. Residents can prevent transients from
settling or immigrating. Residents can drive out offspring and benefit by reduced competition
either through their absence or possible success elsewhere, or both. Residents also could suppress
maturation of offspring and thereby reduce competition, gain benefit through the assistance or
presence of near relatives, or eventually hand over part or all of the resources they control. The
RFH postulates that parents with a high residual reproductive value will benefit in most cases
by forcing their offspring to emigrate.
In this chapter I explore the strategies that seem likely to serve the interests of residents, and
the responses of offspring in the face of these resident strategies. The first step is to review the
context in which the proposed strategies and counter-strategies operate.
Resident Fitness Hypothesis 31
Habitat Heterogeneity
A basic assumption of both the EFH and the RFH is that rodents do not experience habitat
as homogeneous. Instead, spatial and temporal habitat variability create dynamic mosaics on
which behavioral strategies evolve and are expressed. Over the long term in a spatially and
temporally variable environment, an individual’s contribution to the species gene pool is depen-
dent upon the transfer of alleles to other populations (Roff, 1975).
The role of habitat heterogeneity was first given strong emphasis by workers in the USSR
(Fenyuk, 1937). Recently, descriptive models of this sort and their implications have been
discussed by Anderson (1970, 1980), Hansson (1977), Lidicker (1985b), Naumov (1972), Smith
et al. (1978), and Stenseth (1980). The thrust of the concept of habitat heterogeneity is that some
habitat patches are relatively stable over time and support behaviorally defined groups of related
individuals more or less continuously. These patches are “core” or “survival” habitats. Other
patches are subject to wide fluctuations in habitability and are frequently recolonized following
recovery from seasonally predictable or stochastic declines in carrying capacity. These are “‘col-
onization’’ habitats. Patches of the former type could produce the majority of emigrants, whereas
the latter sort, and even less suitable areas, receive most of the immigrants (Anderson, 1970).
The RFH can be understood and its implications worked out only in the context of a concept
of habitat that is patchy in space and time. It is a point of considerable importance that emigration
much exceeds immigration in the more favorable or stable patches (Anderson, 1970; Hansson,
1977). An illustrative comparison of the dynamics of two vole species in three habitat types has
been published by Getz et al. (1979).
Fine scale habitat variability has been described for Microtus californicus by Cockburn and
Lidicker (1983) and Ostfeld et al. (1985). Breeding females aggregated, and individuals remained
in the trappable population longest, in high quality habitat, defined by proportionally high
coverage of a perennial grass. The sex ratio was biased toward females in these high quality
habitats, per-capita reproductive success was high, and immigration was lower than in poor
quality habitats (Ostfeld and Klosterman, 1986).
Although some habitats are of higher quality, and some are more stable than others, neither
quality nor stability are constant. Most rodents about which information is available inhabit
environments that are highly seasonal. As a result, the relative advantage of r-selected or K-se-
lected strategies can vary with the annual cycle. Evolutionary success depends to a considerable
degree on flexibility and on the degree to which bets can be hedged (Stearns, 1976; Stearns and
Crandall, 1981a). The stochastic component of change might be high and dispersal strategies
that generate a degree of serpendipity (Anderson, 1978) would be especially advantageous.
Strategies for Resident Rodents
I assume that residents will maximize their fitness by optimally regulating both emigration of
offspring and immigration of other conspecifics. What factors will be important in the adaptive
strategies of residents toward potential emigrants and potential immigrants?
Parents might benefit through dispersal of their offspring if the latter become established in
more than one habitat patch (Horn, 1983). This could help avoid lineage extinction and permit
the testing of variable offspring in different environments. The higher the risk of local extinction,
the more young should be exported if the benefit is to be achieved. On the other hand parents
might benefit through philopatry of their young by allowing the young to avoid the costs of
emigration, provided the cost of retaining the young does not exceed the benefit of their continued
presence. If, toward the end of a breeding season, parental mortality rates are likely to exceed
those of young, the best parental strategy could be to suppress development of young if this
functions to limit filial competition and thus avoid the need to force their emigration.
Frequent and copious emigration has been commonly predicted for r-selected species, but it
has also been shown that emigration may be adaptive for K-selected species (Hamilton and May,
1977). The probability that parents can benefit by forcing emigration of offspring may vary with
32 Rodent Dispersal
the probability of nearby vacancies. The optimal strategy of residents will also vary with the
qualities of the individual residents, and those of the conspecifics toward whom the resident
strategies may be directed. Residents vary in sex, nature and level of sexual activity, resource
requirements, age, and residual reproductive value. All other conspecifics (including offspring)
are competitors for food, space, and shelter. Conspecifics of the same sex can compete for mates.
Unrelated adults and their young can occupy space that could be occupied to greater advantage
by relatives. Strategies toward offspring are the most complex and the most difficult to analyze.
The concept of inclusive fitness applies to these relationships, but is easily misunderstood
(Grafen, 1982). Ideally, fitness might be defined _as the relative contribution of the alleles making
up.an individual’s genome to the ongoing gene- -pool of the population. Inclusive fitness incor-
porates the incremental (or decremental) influences of individuals on the reproductive success
of kin, multiplied by the degree of relatedness of those kin (Hamilton, 1964a, 1964b). Successful
offspring are the direct measure of parental fitness. They are also, in a sense, merely currency
representing the ultimate wealth (alleles) that determines fitness.
Although the alleles offspring carry are the direct component of parental fitness, offspring are
also subject to the positive or negative influences arising from parental behavior. The important
point is that behavioral strategies that maximize the inclusive fitness of resident rodents require
that social behaviors are determined on the basis of relatedness (e.g., critical resources may be
shared to a greater extent with relatives than with non-relatives). Selection will act on this basis,
favoring behaviors specific to each particular combination. With respect to their offspring,
residents must compromise between maximization of their own reproductive value and gain in
inclusive fitness through interactions with their progeny. As suggested by Armitage (1986b),
resident fitness-could be increased in patchy environments if residents behave so as to retain
relatives, including direct descendants, in the natal area provided advantageous compromises
are possible where parent- offspring and male-female interests are in conflict. On the other hand,
if gain through realization of their own reproductive potential plus inclusive gain from the
reproductive success of their offspring at the natal site is outweighed by loss due to intra-familial
competition, parents can maximize fitness by exporting competing or potentially competing
offspring.
The first step in assessing resident strategy is to consider the choice faced by a resident with
respect to incestuous matings. Should the resident force an offspring of the opposite sex to
emigrate, or allow it to settle as a potential mate? Are inbred matings beneficial because the
resulting offspring are especially closely related to their parents and more likely to behave
altruistically?
Calculations quantifying the options with respect to mating from the point of view of a resident
parent are shown in Table 1. I have used the house mouse as an example and accepted the
estimate that if a mating is incestuous there will be an average loss of approximately 0.56 young
for each 10% increase in the inbreeding coefficient (based on the estimate of inbreeding cost
published by Falconer, 1960a, 1960b). In a parent-offspring mating the inbreeding coefficient
(F) is 0.25. As a measure by which to estimate relative potential increment to parental fitness,
I have used the number of haploid equivalents of the parental nuclear genome (mitochondrial
DNA is not included in my model) contributed to the population gene pool at the time of birth
of the resulting litters. If the parent avoids an incestuous mating, and the offspring fails to mate
(option A), the resulting litter (estimating 5.5 as mean litter size for Mus musculus) is represented
by 5.5 parental haploid equivalents. In an incestuous mating (option B) the proportion of the
parental resident’s alleles represented in each zygote becomes 75% (it’s own 50% contribution,
plus 25% contributed by the offspring). The net gain from this 50% increase in representation,
however, is limited by the assumed inbreeding cost to 11.8%.
The calculation that an incestuous mating is preferable, despite the cost of inbreeding depres-
sion, assumes that the offspring has no other opportunity to-breed. If only options A and B in
Table 1 are possible, a parent would benefit by choosing B, but if emigration of the offspring
results in both parent and offspring mating successfully with “unrelated” partners, option C is
Resident Fitness Hypothesis 33
TaBLE 1.—Gains through proportional representation versus inbreeding cost in Mus musculus, based on
Falconer (1960).*
Mating type and inbreeding coefficient (F) Expected litter size Total resident genomes transmitted**
A. Outbred mating by resident (F = 0) 5.5 (5.5 x 2)/2 =5.5
B. Incestuous mating (F = 0.25) 5.5 — [0.56 x (0.25 x (4.1 x 2) x 0.75 = 6.15
10)] = 4.1***
C. Outbred matings by resident and off- 5.5 x 2=11 (5.5 x 2)/2 =5.5
spring (F = 0) + 0.25 x (5.5 x 2) = 2.75
total = 8.25
_D. Outbred matings but probability of off- 5.5 x 2=11 (5.5 x 2)/2 =
spring surviving and reproducing = + 0.25 (5.5 x 2) x 0.19 = 0.53
0.19 total = 6.03
* Falconer Suinsed 0.56 young lost per 0.10 of inbreeding coefficient.
** A genome is defined here as the equivalent of a haploid set of chromosomes.
*** 10.56 x (0.25 x 10)] = loss due to inbreeding depression.
clearly superior. Option C, however, assumes that dispersal has no cost. Option D is more realistic.
It assumes that the chance of the offspring emigrating, settling, and reproducing (dispersal in
its full sense) is only 19%) Option B (incestuous mating) then remains advantageous (provided
there is no cost due to competition for food, matings, and so forth). A still less favorable option
(not illustrated in the table) would be that the resident did not mate and benefited solely through
reproduction by the offspring. In this case the resident’s genome would be represented by a mere
2.75 haploid equivalents. This option would be advantageous only if the probability of A was
very low.
Dawkins (1979) has pointed out that, as Table 1 shows, independent outbred matings by both
parent and offspring outweigh the proportional gain of an inbred mating in potential total
contribution of parental alleles to the next generation. The situation varies with the sex of the
resident and the mating system. For a female parent, option C gives the best return. In the case
of a male parent in a polygynous social system, mating incestuously need not sacrifice an outbred
mating; the combination of an incestuous mating and an outbred mating are possible, resulting
in 11.65 haploid equivalents.
The resident parent’s “choice” of mating with or exporting an offspring must then take into
account the inherent value and the possible costs. Option D illustrates one such cost (the low
probability that the offspring will survive and reproduce if it emigrates). Other outbreeding costs
include any time spent by an emigrant offspring asa transient and settler, and any recombinational
costs such as the breakup of coadapted combinations. Inbreeding costs include those of com-
petition and inbreeding depression.
The foregoing exercise shows that parental “decisions” respecting strong inbreeding cannot
be regarded as a simple matter of avoiding inbreeding depression. The point I wish to make
most clearly is that proportional gain from incestuous-matings-can legitimately be taken into
account, along with other benefits and costs of possible strategies, and that the strategies of male
and female residents are likely to differ as a result.
“My earlier discussion of parental investment and “parental disbursement” becomes particularly
relevant here. The definition of parental investment (Trivers, 1972; Kleiman and Malcolm, 1981)
requires that parental behavior increases the probability of survival of offspring at a cost to the
parent [as emphasized by Clutton-Brock (1984), it is important to maintain a distinction between
energetic costs in calories expended and reproductive costs in negative effect of breeding on
potential for future survival and reproduction]. If the fitness of a_residentis measured at the
time its offspring reproduce, a resident parent that expended energy (a parental cost) to export
offspring might be facilitating its own further reproduction (at a cost to the offspring). Neither
the parental expenditure of energy, nor the cost to the offspring of its manipulation by the
parent, represent parental investment in Trivers’ sense. They are, however, costs of parental
disbursement and as such are relevant to parental strategies. To be of the greatest possible
34 Rodent Dispersal
advantage to the parent, the expulsion of offspring must maximize the reproductive success of
those offspring that manage to survive the rigors of emigration and transiency and reproduce.
If parenting is a selfish activity in an evolutionary sense, the same kind of argument applies
to other resident options. Suppression of maturation of young by adult (parental) pheromones
has been put forward as an adaptation that functions to force young to emigrate. Is it any less
logical to consider suppression as functioning to limit competition from offspring while the
parent's reproductive value is high, simultaneously conserving the young in the natal area, either
as helpers or to avoid the costs of their premature emigration? If the probability of emigrant
survival is very low, retention of young and either suppression of sexual development or incestuous
mating will be the best strategy. Parents should force offspring of the opposite sex to emigrate,
however, if the cost to the parents’ own reproduction through filial competition exceeds the net
gain of retaining philopatric offspring. The outcome of the equation will be determined in part
by the residual parental reproductive potential (Morris, 1982). Offspring should be exported
when the parent’s residual potential is high relative to a high competitive threat and a low
potential inclusive contribution through the offspring. As parental potential declines relative to
the potential reproduction of retained offspring, parents should behave so as to encourage phil-
opatry. Parental strategy might also vary with site quality. Parents occupying high quality sites
would gain most in fitness by passing those sites on to their offspring. For every resident of a
high-quality site there may come a time for nepotism.
As the young approach puberty, the close parent-offspring relationship weakens and offspring
might be perceived merely as relatives. The behavior of residents can no longer be viewed
exclusively from the perspective of parental investment, but must be considered on the basis of
the impact of competition versus the potential gain through inclusive fitness. Residents, having
fulfilled parental duties, must defend resources required for their own residual reproduction,
provided their former offspring cannot contribute more to parental fitness than can the parents
themselves. In either event, it is important that matters be managed altruistically. As Morris
(1982) suggested, export of propagules should be conducted by the parent in such a way as to
minimize the degree to which the fitness of the offspring is compromised. If young are forced
to leave, it is to the benefit of both residents and their offspring that the parting be peaceful.
Wounding, physical or psychological, represents a potential cost to the offspring’s fitness and is
therefore costly, on average, to the parent as well.
Dispersal (emigration followed by immigration, including reproduction) of a propagule of
either sex, from the parental viewpoint, represents a successful gamble. Is it better to gamble
with sons, or daughters? This will depend on both the cost of the offspring (parental investment)
and the return on a particular strategy (reproductive success of offspring, and any inclusive
contribution to parental fitness). In some mammals males grow much larger than females and
are relatively expensive to produce. This could have a significant effect on parental strategies
(Clutton-Brock et al., 1985; Trivers and Willard, 1973). Even though rodent mating systems are
commonly polygynous, sexual dimorphism in size and morphology is less obvious than in red
deer, and it has been less well studied. Differences in growth rates and body size may not become
apparent until after weaning (e.g., Drickamer and Bernstein, 1972; McClure and Randolph,
1980). However, McClure (1981) found, as predicted by Trivers and Willard (1973), that nu-
tritionally stressed female woodrats weaned more daughters than sons. Male and female offspring
might, therefore, differ in cost to the mother and, on that basis, should be valued differently as
disseminules.
The sex of an offspring can determine the potential benefit of a strategy to parents, the timing
of the return on parental investment, and the odds that the benefit will be forthcoming. Parental
strategies should vary with potential benefit, as well as with the cost of the offspring. Sons and
daughters contribute equivalent quanta (0.25) of the autosomal genomes of each of their parents
to a mating. A daughter has a potential for only a few matings and these will be separated by
intervals of pregnancy and lactation. In polygynous and iteroparous species with a short breeding
season and low post-breeding survival, a successful son is capable of more numerous matings.
Resident Fitness Hypothesis 35
As expressed by Carl (1971), a son completing the dispersal process can make a “jackpot”
contribution to parental fitness. Whether it is more advantageous to export sons, however, will
depend on the relative chances for success of male and female disseminules. If variance in success
of emigrant male offspring is higher than that of females (as it may be if sons move farther,
take more risks, and are less likely to immigrate) export of sons may be no more advantageous
than export of daughters.
Although parental strategies should be conditioned by the return on disbursement of young,
as well as by that on investment in young, I suspect that the average net value of offspring, after
disbursement “decisions” have had their effects, should be equally divided between male and
- female offspring. Fisher (1958:159) concluded that at the moment when parental expenditure
on behalf of young ceases, “the total reproductive value of the males . . . is exactly equal to the
total value of all the females, because each sex must supply half the ancestry of all future
generations of the species.” This same reasoning should apply with respect to disbursement
strategies, and parental disbursement behaviors should be adjusted so as to generate an equal
return, through sons and daughters, in terms of contribution of parental alleles to future gene
pools. If, for example, high potential success of emigrating sons is only partially counterbalanced
by high costs of male emigration, parents should make up the difference by nepotism toward
daughters.
I predict, on the basis of the above, that the strategies by which resident males and females
maximize fitness can be expected to be specific to both the sex of the resident and that of the
offspring. An offspring of the same sex is more likely to compete with a parent than an offspring
of the opposite sex. Offspring are less significant as competitors to their parents prior to sexual
maturity. Therefore it would be advantageous to parents to exercise control over the sexual
maturation of progeny of the same sex. Pheromonal means of regulating maturation of young
might serve as a way of regulating competition and thereby deferring disbursement decisions.
Because transients are less closely related to residents than are the residents own offspring,
they should be prevented from immigrating if the cost of competition with the residents or their
offspring exceeds possible benefits, such as those that might accrue from outbred matings. Fur-
thermore, because resident strategies are specific to the sex of both resident and offspring, the
strategies of male and female residents toward offspring could be in conflict (Armitage, 1982b,
1986b) and it is appropriate to examine separately, and in detail, the strategies by which males
and females allocate young to philopatry or emigration.
Strategies for Resident Males
In a situation where food and cover meet minimal requirements and males contribute little
beyond insemination to the production of offspring, male strategies ought to be founded on
securing and defending copulatory rights to one or more females.
Wittenberger (1980) postulated that mammalian polygyny evolved on the basis of female
sociality. He suggested that female aggregation led to selection for males that successfully
associated themselves with female groups. Matrilineal clusters appear to be common among
rodents (e.g., Armitage, 1986b; Jannett, 1980) and might turn out to be the general rule. Males
of most rodent species should therefore be responsive to female patterns of spacing (Armitage,
1986b; Greenwood, 1980) and male strategies therefore could be expected to vary with female
defendability and with assurance of paternity.
For polygynous rodents, paternal investment is not likely to be supplied at the cost of passing
up additional matings (Trivers, 1972). The benefits of paternal care favor monogamy in only a
few rodent species, such as beavers (Busher and Jenkins, 1985), beach mice (Blair, 1951; Foltz,
1981b), and prairie voles (Getz et al.,1981; Thomas and Birney, 1979).
Defense of space by males is advantageous insofar as it enhances or guarantees exclusive access
to females and assurance of paternity. How does this translate into strategies of resident males
toward male siblings, sons, and male transients? If they can do so, individual males should benefit
by excluding all other sexually mature males. Where individual defense of space is ineffective,
36 Rodent Dispersal
cooperative defense by several related males might still be advantageous, with or without a
dominance hierarchy, particularly if the males forming a cooperative group were relatives and
could benefit through inclusive contributions to fitness. This potential should be highest among
male siblings, or between fathers and sons.
At sexual maturity, male offspring become potential competitors for the limited supply of
copulations available. Because sons are able to contribute only half as many of a male parent's
alleles to a mating as the male parent can contribute, it is likely to be in a resident male’s interest
throughout most or all of his sexually active life to cause sons to emigrate, or to prevent them
from mating if they fail to emigrate.
Resident males have greater cause to repel potential male immigrants than they do to expel
pubertal sons. Potential male immigrants will share fewer alleles with resident males than do
sons, might have the potential to block recently established pregnancies, and might behave
infanticidally toward young sired by a resident male. In the process of establishing themselves,
immigrant males might also cause premature emigration of the resident male's sons. Resident
males should behave so as to repel male immigration during, and in anticipation of, the breeding
season.
The strategy of a breeding male toward daughters should reflect the fact that daughters
represent potential matings. Paternal males will benefit if daughters remain on the natal range
and become sexually mature at an early age. As I have shown, a polygynous male has little to
lose in an incestuous mating even if the high proportional representation of the paternal genome
fails to fully compensate for inbreeding costs. Emigrant daughters represent lost copulations.
Smith (1979), discussing father-daughter mating in fallow deer, has treated incest as a form of
altruistic behavior on the part of the female. Assuming the ability of a male to mate with any
other available female is unaffected by an incestuous mating, Smith (1979) reasoned that in an
outbred population the male risks loss of fitness only if the coefficient of inbreeding depression
is at least 0.33. If persistent inbreeding has reduced the frequency of deleterious lethals, the level
at which a male will lose fitness is proportionately reduced. Daughter success elsewhere lacks
the jackpot potential of male offspring. Therefore resident males should be less likely to cause
daughters to emigrate than sons. a
How should resident males behave toward transient females? In polygynous species resident
males should not inhibit female immigration because transient females represent potential cop-
ulations and these should be free of any inbreeding costs. In monogamous species, behavior of
a mated male toward transient females should be influenced by the degree to which such females
represent threats to previous or future paternal investment.
Implications of Strategies Postulated for Resident Males
A great deal of research effort during the past 35 years has been based on the assumption that
male aggressiveness would prove to be a significant factor in limiting population density. Pos-
tulated mechanisms include death or morbidity arising directly from agonistic interactions (South-
wick, 1955a, 1955b), physiological responses to such interactions (Christian, 1963), establishment
of dominance hierarchies leading to expulsion or inhibition of subordinates (Christian, 1970),
inhibition of immigration (Healey, 1967; Sadleir, 1965), emigration of “surplus” individuals
(Lidicker, 1975), and selective pressures leading to maladaptive shifts in gene frequency (Chitty,
1967; Krebs, 1978a, 1978b). The assumption about male aggressiveness was founded on the
observation that sexually active, unfamiliar males fight when forced to face each other in an
arena. Combat under these peculiar circumstances is a logical outcome of male competition for
copulations but it need not be directly relevant to the behavior of resident males with respect
to sons, or transient males, in nature. The RFH postulates that such combat is abnormal, par-
ticularly where father-son contests are involved.
Contrary to the assumption that has guided so much past research, the RFH predicts that
male aggression will only rarely have a significant restraining influence on population increase.
Population growth in polygynous species could mean that there will be a larger number of
potential copulations available to a resident male. Male fitness would be increased as a result of
Resident Fitness Hypothesis Si)
a local increase in female density and any male behavior that would restrict population growth
would be selected against. In such a scenario males would lose fitness by expelling female offspring
or resisting female immigration. Export of sons and exclusion of transient males would only
partially counter the increase in density through production of young, because young males
‘become competitive threats only at maturity. According to the RFH, resident males should
behave to resist increase in density of related or unrelated females only if shortages of food and
cover threaten prior paternal investment sufficiently to outweigh the gain that would be derived
from increased female availability. Similarly, sexually inactive male relatives should be excluded
only if prior or future investment is threatened by their presence. Male defense of space should
' be more evident in monogamous species because of the value of protecting a relatively high
level of paternal investment in young.
Male aggressiveness might, on the basis of the RFH, have a significant effect on pre-breeding
emigration of males. If females reach estrus more or less simultaneously when a breeding season
is initiated, males can most efficiently attend to the business of locating and mating with receptive
females if mating rights have been settled previously. Male competition prior to the breeding
season could establish a hierarchy with respect to copulatory privileges and/or force emigration
of subordinate males.
Once estrous females cease to be available as the end of breeding activity approaches, and/
or resident males’ residual reproductive values decline, the RFH predicts that male nepotism
toward male offspring should occur. This is because males with low expectations of breeding in
another season would lose fitness by forcing the costs of emigration on sons that might be able
to claim mating rights at the natal site in the new breeding season. Males cannot be certain of
paternity, but if males sharing the same or neighboring space are relatives, tolerance of young
males might extend to all potential close relatives. If resident males would benefit near the end
of their own reproductive lives by tolerating settlement of young males born nearby, any residual
density-limiting effects of male aggressiveness are predicted to decline sharply at this time.
_ Establishment of sons and transient males is predicted to contribute to the end- of-breeding
increase in density.
Strategies for Resident Females
Females are not likely to have to compete for copulations. Instead, resident female fitness may
be limited by competition for the nutritional resources required for gestation and lactation and
for territories that will provide such resources along with secure nest sites for their litters. Females
should choose among potential mates, but because resources can determine the survival and/or
success of an entire litter, females should give priority to habitat choice over mate choice. Further,
paraphrasing a conclusion reached by Alexander (1974), if females make a greater per-offspring
investment than do males, they should be proportionately more influential in controlling the
emigration of those offspring. According to the arguments summarized by Wittenberger (1980),
the behavior of high-ranking females should control the size and composition of any social
groupings.
Because female requirements change over the course of estrus, pregnancy, parturition, and
lactation, female behavior toward potential emigrants and potential immigrants can be expected
to vary with stages of the female reproductive cycle. Emigration induced by resident females
might coincide with the peak of female aggressiveness. This occurs during lactation (Ostermeyer,
1983). In monestrous species and also at the start of breeding in polyestrous species emigration
induced by resident females could result in a well-defined pulse of emigrants.
If female strategy reflects resource needs, resident females should be more responsive than
males to-food-shortage and more active than males in defense of space containing resources.
Perceived or predictable shortages ought to lead females to behave so as to induce emigration
of offspring whose competitive roles outweigh their contribution to maternal fitness. Sexually
active daughters represent a greater threat to resources required by resident females than do
sons. Why, then, are females more nepotistic toward daughters than toward sons? In the absence
of competition for matings or resources, resident females should conserve daughters (i.e., avoid
38 Rodent Dispersal
the loss of fitness inherent in the high risk and low gain emigration equation) and behave
nepotistically toward them. Females ought to induce emigration of daughters only when resource
_ shortage becomes an overriding threat to residual maternal reproductive value. Sons should be
_ preferentially exported when the breeding system is polygynous and at times when the probability
is high that a successful son will mate soon and mate often. If male emigrants have an advantage
in potential total matings and/or dispersion of matings in space, females may respond to resource
shortages selectively, expelling sons before expelling daughters. If the preweaning cost of pro-
ducing male offspring is greater than the cost of producing daughters, maternal females that
respond to nutritional stress by favoring daughters before weaning (Clutton-Brock et al., 1985;
Trivers and Willard, 1973) should behave so as to conserve sons and export daughters after
weaning.
Female strategy should also reflect mate choice. In polygynous species any mating in which
there is a net loss through inbreeding depression will represent a more significant proportion of
a female’s potential lifetime reproductive investment than is the case with a resident male. Sons
will also be less attractive as mates than reproductively proven and familiar males that have
demonstrated their effectiveness as mates and their competitive ability in contests with other -
males. Previous mates are likely to be effective in preventing immigration and reducing any
chance of pregnancy block or infanticide. Therefore, I think it unlikely that females will show
mating preference for sons over older resident males who have sired their previous litters. They
might, however, be likely to conserve sons as future mates in the absence of resident males with
whom they have mated previously. If pair bonding and paternal care are unimportant, females
might also hedge against poor mate choice through multiple paternity of their young, but this
should not significantly affect resident female strategy with respect to expulsion or retention of
young of either sex in the natal area.
Female residents, like males, should expel offspring with as little detriment to the young as
possible. The behaviors encouraging emigration of daughters might promote maternal fitness
most effectively when maternal reproductive value is high and emigrant daughters have the
greatest chance of finding available habitat. It-has been suggested that the optimum time to
export young is when density is low and carrying capacity is expanding (Morris, 1982). At times
of increasing or surplus resource availability, however, the adwantages of maternal nepotism may
be high. Maternal females then may optimize by shifting nest sites or moving to a contiguous
area, if they are better able than their daughters to accept the costs of movement and to establish
themselves on the periphery of their former ranges. Abdication might also be an advantageous
strategy when a female's residual reproductive value is low. Such maternal behavior would serve
to minimize cost to daughters, maximize daughter success, and retain the opportunity for inclusive
gains through further altruism. If abdication is primarily a way of assuring resources to offspring,
females would not be predicted to make such moves to benefit sons.
Resident females have reason to resist incursion of unrelated conspecifics of any sex and age.
Other females and their potential offspring represent the greatest threats to a resident female's
resource base. Resident females should be especially hostile toward transient females, but resident
females should be tolerant of female neighbors and their young to the extent that they are
related.
Resident females also should be aggressive toward male intruders; contact between resident
females and transient males should be limited. To whatever extent experimental induction of
pregnancy block and male infanticide can be extrapolated to nature, unfamiliar males are threats
to current or prior investment. If possession of a home range is a useful criterion for choice of
a mate, transient males should also be repelled as less desirable than established, familiar, resident
males.
Implications of Strategies Postulated for Resident Females
The differences between male and female strategies have significant consequences. The cop-
ulations on which male fitness depends come in discrete and mobile packages (females). The
actual copulatory opportunities are ephemeral. The resources of prime importance to females
Resident Fitness Hypothesis 39
are generally more widely and thinly dispersed, fixed in space, and continuously (though variably)
present and in demand. Therefore the resources needed by females require territorial defense
and are amenable to it. If potential immigration greatly exceeds carrying capacity (Redfield et
al., 1978b), then strong selection for defense of space by females can be anticipated. It follows
that female territorial behavior, because it functions to assure the resource base available for
their own and perhaps their daughters’ reproduction, might be responsive to contacts with
neighbors or transients (perceived density?). The RFH predicts, therefore, that emigration-
inducing and immigration-restricting behaviors of females ought to be more sensitive to crowding
than those of males. Because females have a means (pregnancy) of anticipating increased resource
requirements (during subsequent lactation), female behaviors that induce emigration could rise
prior to attainment of peak density. As resources wax and wane in seasonal environments, female-
governed emigration should show concordant trends.
As potential immigrants of either sex threaten the resource base on which the past, current,
and future reproductive value of a resident female depends, resistance of resident females to
immigration in both monogamous and polygamous mating systems should be effective in pre-
venting increase in population density through immigration. Such resistance might be density
dependent (increasing with perceived density). Territorial behavior of females, when linked to
resource availability, is a potentially significant factor in limiting increase in population density.
The effects of female control of immigration and emigration should be more significant de-
mographically and more complexly seasonal than those of males.
_ The RFH predicts that male immigration, opposed by residents of both sexes, is likely to be
rare. It follows that pregnancy block and male infanticide are unlikely to be of any demographic
significance. .
Conservation of daughters by resident females leads to matrilineal groupings. As a consequence,
the maternal female could benefit by the cooperation of close relatives. The major advantage of
female aggregation in ground squirrels has been thought to be protection against predators
through giving alarm cells that alert kin (Michener, 1983b). On the basis of the RFH it might
be assumed that matrilineal groupings in ground squirrels arise as a result of conservation of
daughters and the inclusive benefits of having amicable neighbors, and that alarm calls are a
secondary development in habitats where predators, and warning calls, can be detected at a
distance.
The common failure to demonstrate density-dependent emigration (Gaines and McClenaghan,
1980) should not be unexpected if only crude density (i.e., total individuals per unit space,
irrespective of sex and age classes) is measured. If the RFH is correct, more intelligible results
should be obtained if sex and age effects are carefully considered, and the relationship between
emigration and density of breeding females per unit of space or per unit of some measurable
nutritional resource is subjected to close examination. Unlike male aggression, female aggres-
siveness should have the potential, under all mating systems, to act as a density-limiting mech-
anism by inducing emigration and preventing immigration.
Strategies for Offspring
To the best of their abilities, offspring must cope with their environments in ways that maximize
their own fitness. The RFH approach views the pre-existing strategies of parents and other
residents as major environmental factors in the context of which offspring are forced to respond.
I emphasize that the topic here is offspring fitness, not emigrant fitness. The latter term applies
only to strategies an individual might adopt as it is forced to emigrate.
To recall another point raised in Chapter I, weanlings, when they leave the nest, cannot be
equated with residents on established ranges. The transition from nestling through weanling,
juvenile, and subadult to established resident is a critical process in the life of an individual
rodent. A home range is established during some period after weaning. We know almost nothing
about the process by which home range and its associated psychological security, social dominance,
and tendency to return if displaced, are acquired. I believe it is extremely important to recognize
that most animals that emigrate are leaving from a natal site, not from a home range.
40 Rodent Dispersal
_Establishment at or near the natal site is likely to be advanlageeus (Jones, 1986). The natal
structed burrows or runways or accumulated food stores; it is an area mrebited by near relatives,
which could benefit by altruistic behavior and which could behave altruistically in turn. The
potential emigrant has some familiarity with the local area. It can have no knowledge of unex-
plored habitat elsewhere. Philopatry avoids costs in energy, time, and risk. Whether or not local
resources have been depleted by use, the natal site has at least some of these advantages over
other areas.
The RFH assumes that the primary strategy for offspring is to behave so as to maximize the
opportunity for philopatry. Philopatry (defined as establishment within breeding distance of the
natal site) might be especially crucial to survival in those rodents that depend on hibernacula
or communal stores for survival through unfavorable seasons. This tendency of offspring to settle
on the natal site, or as near to it as possible, may be in conflict with the interests of residents,
including parents (Horn, 1983).
As Trivers (1974) emphasized, young are likely to be ill-equipped, physically or psychologically,
to contest territorial rights against aggressive and established parents. The young face a dilemma:
confrontation with unrelated conspecifics, whose actions will be unconstrained by the dictates
of inclusive fitness, will be even less likely to be successful. The strategies of young must combine
behaviors that maximize the possibility of local establishment, but also optimize the outcome of
emigration if it is forced on them.
Inbreeding depression resulting from the homozygous expression of deleterious alleles may be
of minor consequence in determining the strategies of offspring. Offspring, like parents, may
gain high proportional representation in the descendent gene pool through incestuous matings.
When such gains are coupled with the advantages of avoiding the risks of emigration, inbreeding
costs are likely to be outweighed.
Given the resident strategies postulated, young may adopt strategies that increase the chance
of philopatry, or they may optimize the timing of their emigration. Conditions may be favorable
for philopatry at the beginning of a new breeding season when there has been overwinter
mortality, at times when resources are expanding (e.g., during the spring flush of growth or
when a new seed crop appears), or when parental reproductive potential has been expended
and parental replacement can be anticipated (Jannett, 1981b). Appropriate delays in maturation
may serve either to avoid emigration and increase the chances of establishment at the natal site,
or to allow an unavoidable emigration at the most favorable time and stage of ontogeny (Frogner,
1980; Morris, 1982; Stearns and Crandall, 1981a, 1981b).
Will competition with siblings affect emigration? If, on average, each parent is to be replaced
by a single young, it is at the time when parental gain through enforcing emigration of young
is waning that competition among siblings may be most significant. This competition could be
for safe hibernacula (some ground squirrels) or for some other resource important to survival
during the non-breeding period. On the other hand, there might be advantage in maintaining
an aggregation over a winter season (Madison, 1984, 1985; Madison et al., 1984).
The RFH predicts that in most seasonal breeders terminal litters should be the most philopatric.
Emigration should cease at this time, and settlers may come from the transient pool as predicted
above on the basis of the relaxation of resident defenses. The high recruitment at this time may
give a false impression that emigration is high.
Is it more advantageous that offspring emigrate singly, or in the company of siblings? If
emigration is “companionate” should the companion be of the same or the opposite sex? Irre-
spective of sex, transients might benefit from companionship of kin through increased tolerance
to climatic stress (i.e., huddling at low temperatures) and reduced risk of predation (i.e., lower
risk per individual). If opposite-sex siblings traveled together, they could avoid mating delay if
available habitat were located. Dispersal with a sibling, as with choice of a mate at the natal
site, would invoke the equation of high proportional representation versus inbreeding depression.
Emigration with a sibling might have significant advantages, although any gains would be
measured by selection against costs such as inbreeding depression or delayed maturity in the
Resident Fitness Hypothesis 41
presence of a familiar sibling. Companionate dispersal might facilitate retention of co-adapted
allelic combinations, and through cooperation siblings might also be more effective in contesting
for territorial rights as has been suggested for lions (Bertram, 1976).
Strategies for Male Offspring
Paternal pressure can be expected as male young approach sexual maturity. Young males are
unlikely to displace either paternal males or-resident-males elsewhere. Delayed maturity may
be a useful recourse. Although delayed maturity incurs a cost in time lost for reproduction, this
cost may be balanced by the benefits of philopatry or of emigrating at an optimal time. A young
‘male that avoids expulsion may eventually replace a resident male parent if the latter should
die or become sexually inactive. Delay may allow for greater physical growth and improve
chances of competitive success.
In seasonally breeding polyestrous species with long breeding seasons, the most favorable time
for male emigration might be determined by availability of females. Space that overlaps home
ranges of females could be available at the beginning of the reproductive season as a result of
overwinter mortality. Females that have not yet become reproductively active at this time might
be less aggressive and might not have established male affiliations. Female availability could rise
again in mid-season as overwintered males die and young females are forced to emigrate.
As the end of the season approaches and the residual reproductive value and sexual activity
of resident adult males decline, philopatry through delayed maturity will become an increasingly
valuable option. In many seasonal breeders, males that overwintered in the previous year are
likely to fail to overwinter a second time. Delayed maturity at the end of the breeding season
(and on through the winter) will allow accumulation and conservation of physiological reserves.
Delayed sexual maturity might not enable young males to avoid maternal pressure. Lactating
females might be especially active in defending resources. A decline in per-capita resources will
bring on emigratory pressure from resident females whethera- male is mature or not. Because
maternal needs for resources for gestation and lactation extend beyond the time when competition
for copulations has ended, the strategy of young males should be to avoid aggressive females
until the last litters are weaned.
At sexual maturity, young males might have a third option, that of persistence in interstices
or on the periphery of ranges of larger breeding males. At least two advantages to such a “floater”
strategy are possible: true emigration and its attendant risks might be avoided, and “sneak
copulations” with resident females might establish bonds that will reduce or eliminate emigratory
pressure from the females, as well as increment the males’ fitness through immediate reproduction.
Implications of Strategies Postulated for Male Offspring
To the extent that male offspring emigrate as a consequence of paternal strategies, the RFH
predicts that their emigration should show little dependence on the density of resident adults.
When young males emigrate in response to female pressure, however, density-dependence might
be apparent (e.g., during a mid-season resource shortage in a seasonally polyestrous species). In
long-lived species such as ground squirrels, female aggression might also generate density-de-
pendent emigration of young males. If female aggressiveness increases with density, it could
operate in such a way as to conserve resources for daughters, or for future litters. In polygynous
species, emigration of young males will have little effect on the birth rate, depressing the realized
rate of increase only through the loss of male emigrants.
Because of the advantages of delayed maturity, young males should often become sexually
mature later in the season than their sisters. In polygynous species, at least, males have the
potential to compensate for delays by numerous matings once the opportunity arrives. Because
it will be to paternal advantage to export maturing sons throughout most of the breeding season, |
emigration of young males would be expected to begin early in the season and to precede that
of female siblings unless postponed by delayed puberty. Emigration of young of both sexes would
be expected to begin concurrently when both are forced to move by maternal pressure associated
with a shortage of nutritional resources. The RFH predicts that in comparison with that of female
42 Rodent Dispersal
siblings, male transiency should be more prolonged, and emigration-associated male mortality
should be higher. In monogamous species, where male investment is higher and paternity more
certain, male offspring should be more successful in settling at the natal site.
In confined situations (island populations or experimental enclosures) the consequences of
blocked emigration of young males will depend largely on the effectiveness of mechanisms
delaying their sexual maturity. If these mechanisms break down, contests with adult males and
among maturing male offspring will lead in the short term (experimental confinement) to fighting
and other behavioral and physiological pathologies, and result in wounding and mortality (pri-
marily of younger males). In the long term (island situations), selection might act against male
aggression and further reduce its demographic impact.
Male emigration might not be very effective in reducing inbreeding. If male emigrants move
the minimum distance possible, and their offspring do this in their turn, inbreeding will remain
high (Bateson, 1983; Moore and Ali, 1984). If males travel farther, export of males might reduce
inbreeding, and parents could benefit through the wider distribution of their alleles.
Strategies for Female Offspring
Like sons, daughters should attempt to remain on or associated with the natal site, especially
if resources are abundant. The RFH predicts that daughters will be subject to maternal aggression
whenever resource shortage and high maternal residual reproductive value coincide, but will
rarely be subject to paternal aggression (perhaps only in monogamous species). Female offspring
should, unless inbreeding costs are overriding, exploit maternal nepotism and settle in, or at the
periphery of, the maternal home range. ‘
Because females commit a significant proportion of potential reproduction to each mating,
however, any net inbreeding cost may weigh more heavily in the balance with the advantages
of philopatry than is the case with their brothers. If so, behavior of young females is more likely
to show evidence of inbreeding avoidance than that of male siblings. When in estrus, young
females would be more likely than their mothers to accept nearby male residents as mates. As
these males are likely to be close relatives (uncles or half brothers) matings will still be inbred,
although less strongly so than with parents or siblings. If any daughters emigrate to avoid
inbreeding, they might leave before male siblings as a result of earlier maturity, but their higher
probability of immigration should lead to shorter dispersal distances. If inbreeding depression is
a deciding factor, philopatry of daughters should also be negatively correlated with residual
reproductive value of male (paternal) residents.
Should daughters be directly sensitive to resource shortage (i.e., respond in the manner antic-
ipated by the EFH) or responsive only to maternal pressure? In general, a resource shortage
should induce maternal pressure earlier than it could induce a response in the young because
resident (breeding) females will have the greatest nutritional demands, the greatest sensitivity
to shortage, and the best basis for detecting resource deterioration. This suggests that maternal
pressure is likely to cause filial emigration before young of either sex have an opportunity to
emigrate spontaneously.
In resource-stimulated emigration, the timing of resource shortage in relation to puberty could
be an important variable. Sexually activated daughters are more threatening to current and
future reproductive investment than are pre-pubertal daughters and more likely to be subject
to maternal pressure. Young females might gain fitness by delaying sexual maturity if the resource
shortage is temporary, or if the maternal female will soon become sexually inactive (at the end
of the breeding season). If offspring (of either sex) delay maturity when there is a mid-season
resource shortage, they could benefit by functioning as helpers in rearing siblings.
The effectiveness of a delayed-maturity response depends on the strategy of the maternal
female. If maternal nepotism is best invested in her last litter, maternal aggression may continue,
or even increase, through her final lactation, then decline abruptly. In this event, daughters
might be under greater pressure to emigrate, relative to sons, than was the case earlier in the
season. Female young in penultimate litters might gain the most by delaying sexual maturity
and/or attempting to persist at the periphery of maternal ranges.
Resident Fitness Hypothesis 43
Once transient, young females should settle in the first unoccupied site where resources are
adequate for reproduction. Proximity to the natal site would minimize delay in appearance of,
and mating with, a male. Although it would reduce the chances of an outbred mating, it would
maximize the potential for altruism on the part of neighbors.
Should female young mate prior to emigration, while transient, after settling, or as part of
the immigration process? At times when the probability of finding unoccupied sites is high,
female young forced to emigrate might gain fitness by an incestuous mating prior to emigration,
or a (presumably outbred) mating while transient. In such matings, fitness would not be reduced
by delay in finding a mate if and when a young female succeeded in settling in available habitat.
‘Unaccompanied pregnant females might commonly initiate populations in new locations under
such circumstances. As long as males are more likely to emigrate than females, however, emigrant
females should have little difficulty in finding a mate.
If most sites were occupied, and if immigration were dependent on acceptance by a resident
male, estrus might enhance the probability that a resident male would accept an unfamiliar
female. Pregnancy block, if it occurs in nature, could have a similar effect. A female could hedge
bets by mating prior to emigration, but having a potential for blocking pregnancy and returning
to estrus on prolonged contact with an unfamiliar male if an opportunity to immigrate could
arise by that means. This, rather than some of the commonly postulated advantages, might be
the selective basis for the pregnancy-block phenomenon. In species where resident males are
aggressive toward unfamiliar females, estrous females might be less likely to be driven out and
might, as the result of copulation, achieve immigration.
Implications of Strategies Postulated for Female Offspring
Emigration of daughters should follow a different seasonal cycle from that of their male
siblings, beginning later in the season and showing greater variation (with per-capita resource
availability) in timing and amplitude. If measures of economic density can be devised, emigration
of daughters ought to show density-dependence in the form of a positive correlation with
competition for resources as perceived by resident adult females.
Because emigratory pressure is predicted to be linked to sexual maturity of daughters only
indirectly (via resource shortage), and because nepotism promotes maternal advantage only so
long as resources are adequate, daughters should be less likely than sons to delay maturity. If
female offspring delay sexual maturity, delay should be associated with a shortage of nutrients
or of space (as representative of nutrient availability). In a seasonally polyestrous species, a point
in the breeding season will normally be reached where selection favors delay until the following
year. The point at which young females delay maturity, like that at which resident females expel
daughters, is likely to vary with resource availability. Both emigratory tendency and sexual
maturation of female offspring might become resource-dependent in the latter part of the
breeding season. When resources are abundant, both maturation of adolescent females and
philopatry might be stimulated and females will remain and breed at or near their natal sites.
This creates a potential for exploitation of surplus resources, and rapid increases in population
density. Reproduction under these circumstances might continue beyond the normal breeding
season (e.g., during “mild” winters or “wet” dry seasons). The RFH therefore includes an
explanation for late-season reproduction by young females. The mechanism should be both
sensitive and responsive to resource availability. Breeding of late season cohorts should be highly
variable in response to environmental conditions. Prolonged breeding and recruitment of these
cohorts into the lores population might generate “plague” densities.
Strategies for Transients
Once an individual has been forced to emigrate it can wander in search of suitable habitat
that is not claimed by a resident, or it can attempt to maintain position as a “floater,” "peripheral
to areas occupied by residents. a
Floater strategy may be advantageous if close relatives behave altruistically, if familiar in-
44 Rodent Dispersal
dividuals are less aggressive than strangers, or if a parent of the same sex is ill or near the end
of reproductive life. Occupancy of marginal areas surrounding any high quality habitat could
offer some_of these advantages. Emigrants might opt, temporarily or permanently, for floater
strategies.
When contact with the natal range has been lost, there will be little opportunity to benefit
through altruism. On the other hand, residents would have little to gain by opposing passage of
transients as long as the latter do not contest resident rights to resources or mates. The optimal
transient strategy m might be-to_avoid residents and marked territories, and settle on the 1e first
available > space. I suggest five reasons for this. First, if a mate is available, time lost from lifetime
reproduction will be minimal. Second, because rodents might prefer mates that are only slightly
different from themselves, mutual acceptability might decline with distance. Third, high-risk
travel through unfamiliar habitat will be ended. Fourth, the possibility that matings will suffer
outbreeding depression as a consequence of hybrid breakdown will be reduced. Lastly, selective
pressures will be more like those at the natal site if the transient is able to settle nearby.
Implications of Strategies Postulated for Transients
The reasoning in the preceding section points to the conclusion that long-distance movement
might be common but long-distance dispersal will be rare. Once the floater strategy has been
abandoned, individuals might wander indefinitely in search of opportunities for establishment.
There may, in consequence, be a considerable transient pool available to take advantage of any
local catastrophe (such as an epidemic or a removal grid) or opportunity (such as a swathed field
of grain) that makes space available. The existence and extent of the transient pool would be
difficult to determine if transients are not highly vulnerable to conventional baited traps. If
members of such a pool are trappable, investigators could get false impressions of immigration
rates or overestimate mortality rates. The most significant quality of such a transient pool would
be its potential to lead to massive increases in numbers whenever environmental conditions
permit mass settling and breeding.
Summary
Because it involves interaction of individuals whose close genetic relationship puts considerable
weight on costs and benefits that determine inclusive fitness, dispersal can best be understood in
a broad context that includes both classical selection and kin selection. Dispersal, in the sense that
it encompasses both emigration and immigration, resembles a game in which established residents
have the advantage and always make the first moves. This leads to the proposal that selection
has generated dispersal phenomena in the first instance through advantage to residents. The
responses of non-residents are secondary. They are the result of selection among offspring and
transients and consist of behavior that is the most effective response to resident strategies. It is
on this basis that I have referred to this way of looking at dispersal as the Resident Fitness
Hypothesis.
The working concepts of the RFH are that rodents are fundamentally philopatric and sed-
entary, that the interests of parents and offspring come into conflict with respect to philopatry,
that dispersal is controlled by behavior of resident adults, and that the maximization of parental
fitness requires “judicious” management of the disbursement of offspring.
Although it is not critical to the RFH, considerable attention was paid to the cost-benefit
balance of inbred and outbred matings and it was concluded that inbreeding avoidance is unlikely
to be the most significant factor in resident strategies or those of their offspring. This conclusion
is in agreement with the views of authors such as Moore and Ali (1984) and Waser (1985), who
have emphasized the importance of competition as a driving force in emigration, but my
examination of competition has been more detailed and more specific. The RFH assumes that
resident males compete primarily for copulatory rights, and that resident females compete
primarily for the resources required for gestation and lactation. Both the strategies of residents
Resident Fitness Hypothesis 45
and the response strategies of offspring and transients are assumed to be conditioned by the
spatial and seasonal patchiness of the environment as experienced by small mammals.
The strategies attributed to residents imply that aggressive behavior of resident males would
oppose male immigration but not female immigration, lead to expulsion of maturing male
offspring for as long as resident males retained high reproductive value, and rarely be responsible
for emigration of daughters. As a result, male aggressiveness might not be an effective restraint
to increase-in-population density. If females respond to resource shortage as the hypothesis
predicts, however, female aggression is predicted to be dependent on economic density and to
have significant density-limiting effects. The hypothesis predicts that as long as resources are
abundant, breeding female residents will behave nepotistically toward daughters, leading to the
formation of matrilineal groups. Nepotism will also be favored when the residual reproductive
value of a female resident falls below that of an offspring. Suppression of maturity by parental
pheromones is favored where it is to mutual advantage to limit intrafamilial competition and
at the same time conserve offspring at the natal site.
The strategies of offspring have been predicted on the basis of three assumptions. The first is
that the greatest advantage lies in “inheritance” of the natal site. The second is that selection
operates on the behavior of offspring as a response to prior behaviors of parents and other
residents. The third is that individuals emigrate when they perceive their personal environments
as intolerable. In the absence of habitat disruption, the environment of a potential emigrant in
a mother-young group could become intolerable when a mother behaves in a threatening (even
though non-damaging) manner toward a weaned offspring. Such an unacceptable personal
environment need bear no relation to the density of the population as measured in demographic
terms. An isolated family group would expel offspring in essentially the same way as one imbedded
in a dense aggregation of family groups.
Failing to establish philopatrically, offspring should behave so as to optimize dispersal. That
means emigrating at the most favorable time and moving as short a distance as possible. The
major tactic available to offspring in avoiding, or timing, emigration is delayed maturation.
Delay postpones competition with residents and/or facilitates benefit through altruism toward,
or from, kin. Suppressed development may increase chances of philopatry, or delay emigration.
The value of the tactic will vary with the nature of the annual reproductive cycle, the point in
the cycle, the residual reproductive values of residents, and the potential for establishment
elsewhere. In polygynous species, a daughter that mates with her father can provide an additional
mating that would not otherwise be available to him. Although incest might carry a net inbreeding
cost, it might also increase the chance of philopatry in species where males defend territories.
The resident fitness model assumes variability in genotypes that influence behavior of residents
but it does not require the existence of discrete polymorphisms specifically controlling tendency
to emigrate. It accounts for both seasonal and interannual demographic patterns on the primary
basis of the responses of resident females to resource availability.
IV
TESTING THE RESIDENT FITNESS
HYPOTHESIS AGAINST
OBSERVATIONS IN THE
LITERATURE
In behavioral ecology, theories as to the way things “ought to be” have tended to outstrip the
empirical data (Bekoff, 1981). If it is true that there is unfounded theorizing about rodent dispersal,
it is also true that there is a veritable avalanche of empirical data against which theory might
be evaluated. The difficulty lies in synthesizing the data to the point where it can be applied to
theory. In the last chapter I attempted to provide a new theoretical base from which to study
rodent dispersal. In this chapter I bring together the available data in a format that explores the
fit of the hypothesis.
The Site Tenacity of Resident Rodents
The RFH requires that breeding adults be sedentary. There is an enormous quantity of trapping
data indicating that for most individuals of most species, home ranges, once established, are
effectively permanent for the duration of an individual’s reproductive life (Behrends et al., 1986;
Blair, 1951; Brown, 1966; Fairbairn, 1978a; Harris and Murie, 1984; Hofmann et al., 1984;
Howard, 1949; Jewell, 1966; Krohne et al., 1984; Madison, 1980a, 1980b; Maza et al., 1978;
Michener, 1979; Sadykov et al., 1985; Watts, 1970; Wolff and Durr, 1986; and many other
authors). Exploration (Shillito, 1963) and scent marking at regular intervals (Bronson, 1976;
Christiansen, 1980; Eisenberg, 1963) continuously reinforce site fidelity. The crucial importance
of a home area is indicated by the remarkable development of homing behavior in rodents, and
the rarity with which displaced individuals settle at the sites where they are released (Dahl,
1967; Stickel, 1968).
As demonstrated by Karlsson (1984), site fidelity may actually be the most precise criterion
for discrimination between subadult and adult social status. Site tenacity and reproduction are
strongly correlated. Pregnancy has been reported only occasionally among apparently transient
animals (Kozakiewicz, 1976; Myllymaki, 1977a). Lactating females occupy permanent home
ranges even in species with precocious young (Rood, 1970). Although in a few cases males appear
to roam widely in search of mates (e.g., Kutenkov, 1979; Linsdale and Tevis, 1951) or shift
breeding areas between seasons (Michener, 1979; Sherman, 1980), male breeding activity seems
always to be based on a home area. The evidence is scant that the successful male ground squirrels
that shift ranges breed elsewhere in the next season and although such shifts have been reported
in some populations (Michener, 1979) they apparently do not occur in others (Davis and Murie,
1985).
In a few species, shifts of homesite within the home range have been observed (Kikkawa,
1964) or range boundaries have varied (Madison, 1980a, 1980b); in a few others females may
make stepwise range shifts following progressively shifting food supplies (Tast, 1966) or after
weaning of litters (Jannett, 1978; Myllymaki, 1975, 1977a). King (1983) reported that female
Peromyscus maniculatus moved nest sites between litters without shifting home range bound-
aries. Lemmings of both sexes move between summer and winter habitats (Kalela et al., 1961).
In my view, adjustments such as these do not constitute dispersal as defined here because they
do not alter the social and genetic milieu. They therefore do not nullify the concept of site
46
Testing RFH 47
tenacity. The evidence is strongly in favor of the view that once residency has been established
persistence at the same site approximates the individual’s ecological life expectancy. Rose and
Dueser (1980) found that more than 16% of voles that met their criterion of residency (three or
more captures) persisted on their grids for at least 35 weeks, and 5% persisted for at least 52
weeks.
Although these lines of evidence support the concept of lifetime site tenacity, there remain:
1) the observation that most disappearances cannot be accounted for; 2) the fact that the previous
history of most transients is unknown; and 3) some evidence of long distance movement by
previously resident animals. Myllymaki (1977a) concluded that the dynamism of the home range
in microtines is so great that the concept of life-long home range cannot be considered realistic.
Lidicker (1985a) suggested that “adult dispersal” is common and Viitala and Hoffmeyer (1985)
also challenged the concept of site tenacity, arguing that it may be absent in Microtus agrestis,
M. arvalis, M. pennsylvanicus, and M. xanthognathus. Porter and Dueser (1986) claimed that
the majority of studies designed to identify “dispersers” have shown that large, sexually mature
individuals frequently emigrate. This assertion was based on removal studies and on the criterion
of large body size at first capture. It is difficult to evaluate these arguments at present. Neither
the removal grid technique nor the body size criterion specifies the age, residency status, sexual
maturity, or social status of transient animals at the time they began their wanderings. Definitions
of “adult” often have been vague or variable. Most available data have been biased by the
relative trappability of larger individuals in live traps. Beacham and Krebs (1980) found that
pitfall traps primarily caught small voles, whereas live traps primarily caught large voles. In an
enclosure, nearly half of the animals caught in pitfall traps never appeared in live traps and
those that did so appeared after a delay of more than a month.
Clear exceptions to the rule that a home range, once selected, is permanent for the life of an
individual are hard to find. When the “adult” categorization has been made entirely on the basis
of body size or sexual activity there generally has been no evidence that the individual was
“adult” in the sense of having had a fully developed site attachment elsewhere. In other instances,
no distinction has been made between range shifts and dispersal in the sense used in the present
discussion. Those studies where appropriate definitions were adhered to suggest that, once es-
tablished, fewer than 10% of residents emigrate. Watts (1970) designed a trapping grid that
covered the entire 27 ha of Marley Wood specifically to detect long-distance movements. Of
341 resident adult Clethrionomys glareolus, only eight dispersed. Correcting for the differences
in trap spacing in the design, Watts calculated that adult dispersal per adult lifetime was 6.2%
for male and 2.1% for female Clethrionomys. With fewer data, his estimate for Apodemus
- sylvaticus was 2-3%. Bondrup-Nielsen and Karlsson (1985) estimated the rate of emigration of
mature female Clethrionomys sp. as less than 5%. Howard (1949) reported a single pre-partum
movement in Peromyscus. Dice and Howard (1951), however, reported that 15% of female and
25% of male Peromyscus bred at more than one site during a single season, with intervening
distances of up to 180 m for males and 442 m for females. Getz and Hofmann (1986) followed
the history of “breeding units” (a pair or trio occupying a specific nest) in Microtus ochrogaster.
In 12% of pairs the partners separated and each moved to a different part of the study area;
16.7% of pairs changed nest sites together. When one member of a pair disappeared, 84% of
females and 64% of males continued to reside at the site following the loss of the partner. Getz
et al. (1987) reported that of 98 such individuals, only 11 acquired new mates. Crawley (1969)
recorded a move of a male Apodemus from one home site to another 150 m distant. Meredith
(1974) observed post-breeding movements of Eutamias amoenus of up to 1 km.
A study of radio-isotope marked Clethrionomys (Sadykov et al., 1985) has produced unusual
data on site utilization. Each “micropopulation” maintained continuous occupation of a stable
core of habitat throughout the year. From this core, voles moved out to forage in a surrounding
area; the extent of the movement depended on season and on favorability of environmental
conditions. In winter, voles fed along the perimeter of the core area, not traveling more than
100 m to feed. At other seasons they foraged out as far as 500 or 600 m. Young of the year
48 Rodent Dispersal
settled in the peripheral feeding zone and fed up to 1,500 m from the colony core when conditions
were favorable. In species whose trap-revealed daily movements were only 5-15 m, excursions
of up to 1,000 m appeared to be typical and possibly routine.
Some young male ground squirrels either emigrate prior to hibernation (Sherman, 1980); others
are driven off the following spring by their mothers (Michener, 1979). Adult males that have
bred in one season move (driven by resident females?) away from the area where they have
bred. Some, at least, might survive to breed a second time. Most of these, but not all (Davis and
Murie, 1985), do not breed at the same site or with the same females in subsequent seasons. It
is not clear that they shift to different demes, nor is it known how many survive and breed again
at a new location. Hoogland (1981) noted that few male black-tailed prairie dogs remained in
the same coterie long enough to mate with their mothers or daughters, although 94-99% of
surviving females remained in the same coterie in successive years. Although 86% of males born
into a colony remained in the natal coterie in their first (non-reproductive) year, most survivors
bred in coteries or wards other than those in which they were born. Careful observation and
analysis of behaviors and post-breeding fates of successful males in these and other diurnal species
will be important in evaluation of RFH and EFH hypotheses.
Despite the questions raised by a few investigators, permanent establishment appears to be a
basic part of rodent life history strategy. Most claims of “adult emigration” are based on inad-
equate and overgenerous definitions of “adult’”’ and/or of “emigration.”
The Prevalence and Importance of Philopatry
The RFH postulates that in most cases in which an individual emigrates, it does so because it
was driven from the natal site by residents, primarily its own parents, and that it would have
remained at the natal site if it had been given an opportunity to do so. It is well to remember
that data are likely to be biased in favor of detecting philopatry. One is most likely to discover
the place of residence of philopatric individuals and least likely to detect establishment elsewhere.
Greenwood (1983) and Waser and Jones (1983) found few exceptions to philopatry. Among
36 species in 12 families for which Waser and Jones (1983) found published data, clear evidence
of philopatric tendencies was lacking only for males of two sciurid and two cricetid species.
Jones (1986) found that of 147 young Dipodomys spectabilis that became established, 24 males
and 13 females acquired their natal mounds. Young of both sexes remained in the natal mound
until able to occupy vacant sites nearby. Seventy-nine percent of 97 male juveniles and 77% of
99 female juveniles settled within 50 m of natal sites or points of first capture. The median
dispersal distance in this species was 17 m for males and 30 m for females. Among individuals
eventually successful in establishing themselves, survival over the first post-establishment year
was 50% higher among philopatric settlers than among those settling elsewhere (Jones, 1987).
Disappearance of either parent increases the probability that an offspring of that sex will be
successful in establishing residence (e.g., Dickman et al., 1983; Dixon, 1958; Slade and Balph,
1974; Svendsen, 1980). It has yet to be demonstrated, however, that all young will settle on the
natal range if not actively expelled.
Given a general and presumably inherent tendency to philopatry, success rates vary. Most
data show the expected bias in favor of females. Dice and Howard (1951) found that 38% of
female and 28% of male Peromyscus maniculatus settled at their natal sites. Mean breeding
distances of 10 male and 10 female P. leucopus were 75.5 and 39.3 m, respectively, from known
birth sites (Goundie and Vessey, 1986). Wolff and Lundy (1985) reported that some overwintering
groups of P. leucopus and P. maniculatus consisted of mothers, offspring, and possible fathers;
most also contained individuals not known to be relatives. By spring all the autumn-born male
P. leucopus had disappeared from their natal ranges, but 30% of autumn-born females bred
within the range of a possible father. Three of seven male and two of eight female P. maniculatus
bred within their natal ranges in the spring following their birth (Wolff and Durr, 1986). Baker
(1981b) found that less than 1% of house mice living in chicken coops moved between buildings;
individuals carrying an introduced allele tended to be located near their putative mothers.
Testing RFH 49
Mackin-Rogalska (1975) examined the fidelity of Microtus arvalis to family burrow systems in
an enclosed 1-ha field. She concluded that fidelity to a burrow system was not apparent among
males or in young born early in the season. However, she did not consider possible disruptive
effects of confinement. Stoddart (1971) observed that recruitment was largely philopatric in
Arvicola terrestris. He reported that early season young were philopatric, but those born after
1 July were not. Female Clethrionomys rufocanus settle as close to the natal site as possible and
as long as density is low matrilines are discernible (Viitala, 1977; Viitala and Hoffmeyer, 1985).
Kawata (1985a) found greater heterogeneity in frequencies of electromorphs of female than of
male Clethrionomys and attributed this to greater philopatry in females. According to Getz and
Carter (1980), most female Microtus ochrogaster that succeeded in establishing home ranges
did so within 30 m of their natal nest. Among young M. ochrogaster that survived to the age
of maturity, 68% of males and 75% of females occupied their natal sites for their entire lives
(Getz and Hofmann, 1986; Getz et al., 1987). Although male dispersal distances are greater in
most species, long-distance dispersal in D. spectabilis was biased in favor of females (Jones, 1987).
Female philopatry is very strongly developed in ground squirrels (Armitage, 1984; Hoogland,
1981; Michener, 1983b; Sherman, 1980). More than 60% of female yellow-bellied marmots in
harems were found to remain in the colonies into which they were born, but the proportion of
males doing so was extremely low (Schwartz and Armitage, 1981). At 60 days of age 92% of
female Spermophilus beldingi, but only 26% of males, remained in their natal areas (Holekamp,
1984).
Data showing the relevance of philopatry within superficially homogeneous habitat have
recently been provided by Cockburn and Lidicker (1983). Within continuous grassland, variations
in habitat quality between areas the size of individual home ranges in Microtus californicus
made a significant difference in individual persistence and reproductive success.
Shields (1983) reviewed various models explaining the trend to philopatry among higher
vertebrates. He rejected models based solely on low vagility, and regarded as more powerful
those models that took into account the risks of movement, the ability of individuals to function
efficiently in a familiar area, the value of local adaptation, and the compatibility of alleles in
local gene pools. In his view, philopatry should prevail in organisms in which the environment
is relatively coarse grained, although wide distribution of propagules would be beneficial if
habitats were ephemeral. Both of these criteria apply to rodents, and the resulting contradiction
might be resolved through the bias toward male emigration and greater male dispersal distances
in the majority of species.
Specific studies that would determine whether philopatry is an inherent and universal tendency
are lacking, although the available evidence is favorable to that view. New techniques (e.g.,
Dickman et al., 1983; Sheridan and Tamarin, 1986; Tamarin et al., 1983; Wolff and Lundy,
1985) are becoming available for identifying litters and following their dispersal. These show
promise of greatly improving our ability to determine paternity, to distinguish among philopatric
individuals, emigrants, and transients, and to determine patterns of dispersal. I expect them to
confirm that philopatry is an innate tendency in rodents.
Discrimination Among Relatives, Associates, and Transients
Because it places emphasis on parent-offspring interactions and inclusive fitness, the RFH
depends on evidence that residents make social discriminations among familiar individuals (mates,
neighbors, offspring, and parents); between familiar individuals and strangers; and between in-
dividuals that are transient and those that are resident. The RFH relies heavily on mutual
recognition among relatives (adults and their own offspring), and requires that adults (males at
least) detect the onset of puberty in their young. Discriminatory abilities are also fundamental
to nepotism; to preference for, or avoidance of, inbreeding (Holmes and Sherman, 1982; Hoog-
land, 1982); and to exclusion of non-kin and “judicious” selection of whether (and when) to
allow philopatry or to force emigration of kin. Do rodents have the required discriminatory
abilities?
50 Rodent Dispersal
Recognition of conspecifics and discrimination of their sexual and social status is based primarily
on odor in rodents (Schultz and Tapp, 1973; Stoddart, 1976). Odors serve to announce stages of
sexual development and activity to conspecifics of all ages and to regulate intraspecific behaviors
(Bronson, 1979; Brown, 1979; Fass and Stevens, 1977; Ropartz, 1977; Stoddart, 1974; Thiessen
and Rice, 1976; Whitsett et al., 1979). In Mus musculus both individual and group recognition
on the basis of odor have been demonstrated. Dominant individuals produce odors different
from those of subordinates, and urine of dominant males contains an aversive factor lacking in
the urine of subordinate males. Stressed individuals emit distinctive odors; female odors tend to
inhibit aggression by males (Ropartz, 1977). Stoddart (1977) showed that sebaceous secretions
of young differ from those of adults in Apodemus and Arvicola, and that the secretions of young
males closely resemble those of adult females (a camouflage inhibiting adult male aggression?).
In Arvicola terrestris, Stoddart et al. (1975) showed by means of gas-liquid chromatography that
flank gland secretions differed between sexes, between adults and juveniles of each sex, between
families reared under identical laboratory conditions, and between populations in the field. They
also suggested the existence of olfactory dialects. Wolton (1984) showed that Apodemus sylvaticus
of both sexes could be trained to discriminate between odors of urine or feces of two conspecifics
of either sex. Much remains to be learned about the role of scent, but it is clear that there are:
1) olfaction-based responses to social and sexual status; 2) adaptations for chemically marking
territories; and 3) correlations between olfactory familiarity and agonistic interactions.
On what basis does olfactory discrimination among relatives operate? Holmes and Sherman
(1982) and Blaustein (1983), viewing recognition as functioning to regulate nepotism or balance
inbreeding and outbreeding, have considered four possible mechanisms on which kin recognition,
nepotism, or inbreeding avoidance (or preference) might be based: 1) individuals might recognize
kin through proximity to the home range or natal site; 2) recognition might be based directly
on association in the natal nest (Porter et al., 1978, 1981, 1983; Porter and Wyrick, 1979); 3)
recognition could be ascertained by phenotype matching if an individual compared its own
phenotype (morphological, olfactory, or behavioral), or those of familiar relatives, with that of
an unknown; and 4) there could be a direct (unlearned) response to “recognition alleles.” Ya-
maguchi et al. (1981) and Yamazaki et al. (1976, 1980) presented data interpreted as showing
that relative to identical females, male Mus preferred females whose genotypes differed from
their own at the H-2 locus. Nevertheless, Holmes and Sherman (1982) concluded that use of
recognition alleles was doubtful and might be impossible to demonstrate.
Empirical data (Gavish et al., 1984; Godfrey, 1958; Grau, 1982; Halpin, 1978, 1981; Kareem,
1983) suggest that both experience and genetic similarity might be involved in kin recognition.
Maternal and sibling recognition might be established shortly after birth (Porter et al., 1978;
Quadagno and Banks, 1970; Stoddart, 1976) or might require several weeks (Michener, 1983b).
Michener (1974) noted that recognition was mutual between maternal Spermophilus richardsonii
and their own young before young opened their eyes, but she has subsequently emphasized that
individual recognition (as opposed to discrimination between familiar and unfamiliar conspecifics)
has not been demonstrated in ground squirrels (Michener, 1983b). Recognition persists over long
periods of inactivity in hibernating species (Michener and Sheppard, 1972).
Laboratory studies provide both direct and circumstantial evidence that extends the functional
importance of recognition. Physiologically, pregnancy can be terminated by intense and pro-
longed contact with non-stud males or their pheromones (Bronson and Eleftheriou, 1963; Bruce,
1959; Chipman and Fox, 1966a, 1966b; Jannett, 1979; Stehn and Richmond, 1975). Similarly,
young can have sexual development activated or accelerated by contact with unfamiliar adults
of the opposite sex (Bronson, 1979; Carter et al., 1980; Milligan, 1980). In confinement, newly
parturient female voles discriminate between males with which they mated and other males,
behaving amicably toward stud males but persistently attacking non-stud males. The latter will
kill young that they have not sired (Mallory and Brooks, 1978, 1980). In contrast, stud males are
unlikely to attack their own young when introduced to the natal cage under these conditions
(Labov, 1980; vom Saal and Howard, 1982). I suspect that infanticide by non-stud males may
be induced by maternal aggression in a confined space.
Testing RFH 51
Reviews of the topics of sibling recognition (Bekoff, 1981) and mother-young recognition
(Gubernick, 1981) have concluded that recognition is learned, but as Blaustein (1983) pointed
out, the empirical evidence for recognition mechanisms remains compatible with both learned
and unlearned recognition. Non-learned recognition could, for example, be based on glandular
secretions (Stoddart, 1976), but learning, on the basis of self-perception, would be difficult to
rule out. Holmes and Sherman (1982) found that sibling Spermophilus beldingi and S. parryii
reared apart differed from non-siblings in interactions when encountering each other for the
first time in a test situation, but Holmes (1984) did not find evidence for such “innate” discrim-
ination in S. tridecemlineatus. He concluded that differential responses of S. tridecemlineatus
in arena encounters could be fully explained on the basis of familiarity. As Holmes (1984) pointed
out, however, the methods varied somewhat and exact comparisons are not possible among
various species. Grau (1982) seems to have demonstrated discrimination of kin independent of
prior contact in Peromyscus leucopus, and a recent study by Porter et al. (1984) also argues
strongly for a non-learned component. Comparisons of responses of P. leucopus to familiar and
unfamiliar siblings and non-siblings in paired arena encounters appear to demonstrate an ability
to discriminate between related and unrelated strangers housed in identical conditions, the
responses to unfamiliar siblings being more cohesive and amiable than those to unfamiliar non-
siblings. Females reacted cohesively toward unfamiliar, related males (more approaches and
more investigation, but no difference in time spent huddling) and aversively toward unfamiliar,
unrelated males (more chases). There were marked differences between male and female response
patterns: males behaved most positively toward familiar relatives, less positively toward unfa-
miliar relatives, and least positively toward unfamiliar non-relatives; females displayed positive
interest most strongly toward non-familiar relatives. Davis (1982) cross-fostered Spermophilus
richardsonii within 24 h after birth. After being isolated for 110 days, beginning 1 week after
weaning, the test animals demonstrated recognition of biological siblings in arena tests, behaving
more cohesively toward siblings than toward non-siblings. Holmes (1986a) showed that female
S. beldingi were less agonistic in their interactions with unfamiliar kin than with unfamiliar
non-kin. These results seem most compatible with a phenotype matching hypothesis.
De Jonge (1983) found evidence of species differences in response to relatives among microtines.
When tested in laboratory arenas at 6-10 weeks of age, Microtus arvalis that had been separated
from their siblings within 24 h of birth investigated siblings without any fighting, but fought
with non-siblings. M. agrestis, under the same regime, fought with both siblings and non-siblings.
Whatever the mechanism, the general trend in discriminatory behavior is toward more am-
icable relationships with familiar individuals of either sex, whether relatives or neighbors. Res-
idents tolerant of associates have been reported to be aggressive toward unfamiliar conspecifics
that are experimentally introduced in both laboratory and natural environments (Anderson and
Hill, 1965; Armitage, 1974, 1975; Armitage and Johns, 1982; Eibl-Eibesfeldt, 1950; Fairbairn,
1978b; Healey, 1967; Hill, 1966; Lidicker, 1976; Reimer and Petras, 1967; Rowe and Redfern,
1969, Sadleir, 1965).
Given that rodents are capable of making fine discriminations among conspecifics, much
remains to be learned as to how the observations on olfactory discrimination relate to social and
reproductive structuring. McLean (1982) found that immediate neighbors among breeding fe-
male Spermophilus parryii were not closely related. However, females that were closely related
tended to move newly emerged young into common burrows whereas distantly related females
did not. Close female kin also had more overlap among home ranges and interacted more
amicably than did less closely related females. Distant relatives that had not associated as young
were intermediate between close kin and non-relatives in these respects. McLean postulated that
aggregating behavior might enable cousins to learn to recognize each other and thus serve to
facilitate extended nepotism. Armitage and Johns (1982) found that among yellow-bellied mar-
mots, mother-daughter and sister pairs were more amicable than expected on the basis of
frequency of occurrence of such pairs in the population.
Carefully integrated field and laboratory observations by Jannett (1980) showed that parous
female Microtus montanus tolerated the presence of only their own young and familiar males
52 Rodent Dispersal
within their home ranges. In monogamous stocks of M. ochrogaster confined in extensive artificial
runway systems, Getz and Carter (1980) observed that all members of any social group attacked
experimentally introduced subadults of either sex, but that the breeding male was the most
aggressive toward both male and female strangers.
Recognition of neighbors, per se, has yet to be investigated adequately. Healey (1967) observed
that male Peromyscus maniculatus were less aggressive toward neighbors than toward strange
males. Vestal and Hellack (1978) reported that P. leucopus behaved less agonistically toward
neighbors than toward strangers in laboratory arena encounters, but failed to observe equivalent
discriminatory behavior in P. maniculatus. Madison (1980a) noted evidence that microtines,
when placed in arenas, are less aggressive toward neighbors than toward strangers; in large semi-
natural enclosures, however, territorially established resident Microtus tolerated introduced
strangers (“transients”) but attacked neighbors at territory boundaries (Skirrow, 1969). Female
Clethrionomys have been reported to be tolerant of neighbors and aggressive toward unfamiliar
conspecifics (Viitala and Hoffmeyer, 1985). Getty (1981) observed general overlap among chip-
munk territories, in conjunction with avoidance of actual contact, and concluded that territorial
behavior was primarily important in deterrance of immigration by non-neighbors. At this point
it appears that neighbors are probably recognized as distinct from transients, but the consequence
may vary with the degree of relationship, the species, and a number of other variables. Like
other interactions, those among neighbors are likely to depend on the sex of the participants.
Armitage (1982b, 1986b) suggested that because males and females compete intrasexually for
different resources, overall rodent social systems actually are composed of separate but inter-
locking male and female systems.
Recognition of offspring by males, or of paternal males by offspring, has been little studied.
Males of many rodent species do not share nests with females and young and thus there would
seem to be less opportunity for discrimination based on close contact. Paternal males are actively
excluded from the nest by the maternal females in some cases. However, if young acquire the
maternal scent, and males respond positively to the scent of females with which they have
copulated, male recognition of offspring could be facilitated. In some caviomorphs, where males
do not share the nest and the maternal females are aggressive toward even stud males, males
take advantage of the females’ absences to scent-mark their offspring (Kleiman, 1977).
Although much remains to be learned as to the basis and function of recognition mechanisms,
the discriminatory abilities of rodents appear adequate to meet the demands of the RFH.
Cohesiveness Among Kin
Emigration and immigration might be greatly influenced by whether kin repel or attract each
other. Repulsion might result from high inbreeding costs, whereas attraction might result from
opportunities to accrue fitness through altruism or positive assortative mating. Hamilton (1964a,
1964b) predicted that the advantages of positive response among kin would cause parents to
behave so as to minimize competition among their offspring.
Familiar odors generally evoke positive responses, and this persists after weaning. In laboratory
tests, young rodents show preferences for odors with which they are familiar (Carter and Marr,
1970; Marr and Lilliston, 1969). Stoddart (1982) found that Microtus agrestis preferred traps
with their own odor over those scented with the odors of other voles. Gubernick (1981) reviewed
the literature of parent-offspring recognition in Rattus, Mus, and Acomys, and concluded that
young learn to recognize their mother on the basis of olfactory and gustatory perceptions, and
that innate parent-offspring attachment was not required to explain the observed patterns.
Evidence of cohesion and cohesive behavior among kin has been found in both laboratory
and field studies. Sibling Acomys were more likely to share a food source and more active in
exploring novel environments than were non-siblings of the same age (Porter et al., 1980). Savidge
(1974) observed that young Peromyscus maniculatus that had been ejected by their mother
tended to travel together when they crossed a barrier. In arena tests, female Peromyscus inves-
tigated unfamiliar sibling males and chased unfamiliar non-siblings (Grau, 1982). Grau’s inter-
Testing RFH 53
pretation was that females investigated the unfamiliar siblings in order to avoid incestuous
matings.
For both Mus (Lidicker, 1976) and Peromyscus (Howard, 1949; King, 1983; Madison, 1977),
there is evidence that littermates associate and travel with parents and siblings later in life. A
tendency for opposite-sex littermates to disperse together has been observed in Peromyscus
polionotus (Smith, 1968). Field evidence indicates that unrelated Peromyscus tend to avoid
association. King (1983) found unrelated Peromyscus together in only 7.5% of 598 observations
of groups. Litters were more cohesive in fall, whereas juveniles were most likely to be encountered
alone in spring and summer. Among 10 male and 10 female emigrant P. leucopus followed by
Goundie and Vessey (1986), there was evidence of cohesion in one litter and no evidence of
active avoidance among littermates in the others. Patton and Feder (1981) found no evidence
of cohesion among kin in pocket gophers colonizing a trapped-out area.
Lidicker (1976) found that Mus released into large outdoor enclosures established and main-
tained kin groups, despite the pressure of very high densities. Genetic evidence showing that
similar group individuality and integrity was maintained in unenclosed populations (Selander,
1970a) demonstrates that kin grouping was not an artifact of confinement.
Sibling cohesiveness apparently varies with species in voles. After a period of separation,
Microtus arvalis behaved affiliatively toward kin even in an unfamiliar environment, but M.
agrestis showed no evidence of affiliative behavior toward kin (De Jonge, 1983). Overwintering
groups of M. pennsylvanicus are formed among kin. Reduction in relatedness within such groups
appears to be a consequence of predator pressure rather than loss of group cohesion. Infusion
of unrelated individuals follows loss to predators because lone individuals join depleted groups,
taking advantage of huddling to protect themselves from the stress of low temperature (Madi-
son, 1984, 1985; Madison et al., 1984). Getz (1972) did not find any evidence that sibling M.
pennsylvanicus behaved cohesively during emigration, and Wilson (1982) reported that sibling
M. pennsylvanicus behaved less cohesively under the same conditions than did M. ochrogaster.
The evidence of greater cohesiveness in M. ochrogaster seems paradoxical with respect to female
reproduction if association with unfamiliar males is required for sexual maturation and if, as
Carter et al. (1986) report, natal territories are rarely visited by unrelated males. It is unclear
how cohesiveness evolved in this species if it inhibits reproduction. Hilborn (1975) and Beacham
(1979b) obtained data that they interpreted as indicating that littermate M. townsendii might
emigrate synchronously, possibly in company.
Formation of kin-clusters as a result of amicable and cohesive behaviors among related females
is evident to some degree in all the well-studied terrestrial sciurids and is most marked among
females (Armitage, 1986b). In Marmota flaviventris, relatedness increased the amount of the
foraging area shared (Frase and Armitage, 1984). However, cohesiveness might depend on
philopatry and continued association. When a group of eight juvenile marmots were introduced
into a new and unoccupied habitat, kinship was unrelated to the frequency of social interaction
(Armitage, 1982a).
Young Spermophilus richardsonii behave cohesively toward the female parent and submis-
sively toward other adults (Michener, 1974) and establish site-specific dominance over non-kin
in the season of their birth. Less physical spacing is maintained between kin than between non-
kin. Amicability toward kin is maintained into the first breeding season, and kin-clusters result
(Michener, 1981). Waterman (1986) observed that on emergence juvenile female S. columbianus
differed from males in greeting the mother more often, playing preferentially with sisters, and
staying nearer the natal burrow over the first 10 days. Related female S. parryii might actively
facilitate cohesion by transporting their litters to communal burrows just prior to weaning
(McLean, 1982). Cross-fostered ground squirrel pups reared together behave cohesively (Holmes
and Sherman, 1982) as do cross-fostered Microtus pups (Gavish et al., 1984). Female ground
squirrel sibs reared apart, however, also show less aggression in dyadic laboratory encounters
than similarly reared non-sib females, providing evidence that both association in early life and
relatedness per se may be involved in cohesion of kin (Holmes and Sherman, 1982). Holmes
54 Rodent Dispersal
(1986b) reported that half-sib S. beldingi females were less antagonistic toward each other than
comparable unrelated yearlings, but that this difference was not evident in male-female or male-
male pairs. Hoogland (1986) found that both male and female Cynomys ludovicianus interacted
more amicably with kin than non-kin. Nepotism was least among males during mating and least
among females at the time when competition for burrows was at its peak. Even when competition
was most intense both sexes were more amicable toward kin than non-kin.
Schaller and Crawshaw (1981) observed that capybaras (Hydrochoerus hydrochaeris) formed
large aggregations during the dry season. Within these aggregations, groups that presumably
consisted of relatives or families maintained their integrity. Young followed their mothers for
up to 1 year after birth.
It appears that cohesion develops in the nest in most species and thus is most probable between
mother and young and among siblings. Among siblings, cohesion is more evident than repulsion.
Familiarity facilitates cohesive behavior; cohesiveness, maternal nepotism, and philopatric ten-
dencies of female young can all contribute to development of matrilineal groupings in the field.
The picture is much less clear with respect to male-female and male-male cohesion and its
relevance to formation of new colonies and to co-dispersal of siblings. Investigators have shown
so little interest in cohesion between males, between fathers and daughters, or between brothers
and sisters that there is a temptation to assume that it is nonexistent. There are, nevertheless,
some suggestions that male siblings emigrate together, and further investigation of inter- and
intrasexual cohesiveness among emigrants would be useful. It would also be useful to know if
relatedness was high among males sharing common or overlapping home ranges.
Mating Preferences of Residents
Sexual dimorphism in body size is less obvious in rodents than in many other mammals, a fact
that might be taken to indicate that sexual selection is weak or absent. As Blaustein (1981) has
emphasized, however, chemical dimorphism (differences in odor between males and females) is
marked. Scent differences among males could provide an adequate basis for expression of mating
preference by females.
Studies of mating preferences in laboratory Mus were reviewed by D’Udine and Alleva (1983).
A number of generalizations can be drawn from their review. Sexual behavior might be less
labile than other forms of social interaction. Relative to females, males tend to be less discrim-
inating in sexual preferences and less fixed in such preferences. Expression of preference by
female Mus is dependent on an opportunity to associate with the father in the nest. Laboratory
strains vary in expression of preference, and females might show preference for familiar males
or for males of slightly different genotype, as opposed to either closely or distantly related
individuals.
Unfortunately, tests of “preference” in many experiments demonstrate only that females
preferentially investigated odors of unfamiliar males. Preference measured in this way might
reflect sexual attraction, curiosity, or aggression. On the basis of such experiments, Hayashi and
Kimura (1983) reported that female laboratory Mus showed no preference within male com-
binations of unfamiliar related, unfamiliar unrelated, and familiar related males in terms of time
spent in neighboring compartments. Even where mating occurs in choice experiments in the
laboratory, results cannot be extrapolated directly to mating in the field because the choice is
limited in too many ways by the experimental conditions. Hayashi and Kimura's conclusion that
the choice of mate is made mainly or entirely by males is unjustified.
In nature also, mate choices by females are likely to be limited. The factors include residency
of females, male residency and territoriality, and male social hierarchy. Jannett (1981a) reported
that in a population of Microtus montanus only those males that occupied territories achieved
physiological readiness to breed. Webster and Brooks (1981) observed in the field that a large
male M. pennsylvanicus remained near a post-partum female for several hours. When other
courting males attempted mounts, the female vocalized loudly and the large male drove off the
Testing RFH 55)
intruders. Kawata (1985b) was unable to find strong evidence that female Clethrionomys ru-
focanus exercised preference, yet in cases in which paternity was determined there was no
instance in which a female had been inseminated by a transient male or by a resident male
whose home range did not overlap hers. R. J. Wolff (1985) reported that in house mouse colonies
founded in the laboratory with an adult pair and a juvenile male, the adult males were dominant
and continued to monopolize copulations until eventually killed by younger males. Thereafter
several individual male offspring were able to establish territories within the colony room. Only
those males that established territories were able to mate. Mating and parturition took place
primarily within the higher quality territories.
Agren (1984b) studied pair formation in Meriones unguiculatus in outdoor enclosures. Females
expressed preference (for males and/or territories) only after males had established territories.
Females then developed their own site-related dominance. Males subsequently became aggressive
toward non-resident females. Females, however, wandered widely when in estrus, and mating
was not restricted to cohabiting males. Agren suggested that females might use male possession
of a territory as an index of male quality. One possible further interpretation is that the presence
of a male is viewed by the female as a component of habitat choice, and subsequent mate choice
is a separate process. Behrends et al. (1986) observed that female Dipodomys merriami wandered
much more widely when in estrus, and Viitala (1977) reported similar behavior in Clethrionomys
rufocanus. Such behavior supports the suggestion of Cox and Le Boeuf (1977) that females
behave so as to incite male competition. Receptivity of estrous females toward males occupying
adjacent home ranges is suggested by the “estrous runs” reported by Viitala (1977), and by
evidence for multiple paternity in Peromyscus reported by Birdsall and Nash (1973). Multiple
matings might also serve to lower the risk of a poor mate choice or reduce inbreeding cost.
Female Belding’s ground squirrels normally mate with several males (Hanken and Sherman,
1981; Holmes and Sherman, 1982), but it is not clear how general such bet-hedging behavior is,
nor whether there is any preference based on relatedness.
How precise can mate choice be? Lenington (1983) reported evidence that female Mus showed
preference for males homozygous for wild-type alleles over those heterozygous at the t-locus.
She found, in arena experiments, that the preference of heterozygous females was stronger than
that of those females that were homozygous for the wild-type allele and had less to lose by
mating with a male heterozygote. Heterozygous males, however, were dominate over male
homozygotes and the high levels of aggression in the experimental context affected female
behavior, introducing uncertainty as to how the evidence for female choices should be interpreted.
In another experiment females showed preference for the odor of homozygous males in a choice
chamber. It is difficult to judge the relevance of these interesting results to the natural context.
There may be considerable variation among species in mate choice. Webster et al. (1982)
investigated copulatory preferences in female voles under laboratory conditions, including re-
inforcement of preferences by successful copulations. When given access to both a male with
which they had just mated and an unfamiliar male, female Microtus ochrogaster showed pref-
erence for the stud male, whereas female M. montanus showed no preference. When separated
for 2 weeks by a wire mesh barrier from a male in the same cage, female M. ochrogaster showed
no preference when given a choice between the familiar male and a stranger, whereas female
M. montanus spent more time with the unfamiliar male.
Behavioral response to an unfamiliar conspecific usually takes the form of an aggressive
approach by a resident. Aggression by resident females toward unfamiliar males has been observed
in Neotoma (Fleming, 1979) and Microtus (Jannett, 1980). Such aggression presumably reduces
the chances that mating will take place. Getz et al. (1981) found that female Microtus ochrogaster
in post-partum estrus vere receptive and non-aggressive toward previous mates, and less receptive
toward unfamiliar males. Reversal of this preference required several days.
Mate cheice in M. ochrogaster is especially interesting in view of the tendency to monogamy.
Although virgin females investigate only the ano-genital odors of unfamiliar males, once a female
56 Rodent Dispersal
has been activated and enters her first estrus she is equally likely to mate with a familiar or an
unfamiliar male. This initial mating establishes a pair bond. Females living in established pairs
attempt to avoid matings with unfamiliar males (Carter and Getz, 1985; Getz et al., 1981).
Dominance status of males seems to be an important factor in female choice in many rodent
species. Female preference for dominant males, or a preferential tendency to investigate odors
of dominant males, has been reported in Mus (DeFries and McClearn, 1972), Clethrionomys
(Hoffmeyer, 1982), and Lemmus (Huck and Banks, 1982a, 1982b). Shapiro and Dewsbury (1986)
found that female M. ochrogaster spent more time near dominant males than near subordinate
males, both when the males were tethered and when separated from them by wire mesh walls.
Under the same conditions female M. montanus showed no preference. In most studies dominant
males have been observed to copulate earlier and more frequently than subordinates. Hyde and
Sawyer (1977) suggested that variation in female aggressiveness over the estrous period might
broaden mate choice (i.e., selectivity might be reduced during estrus as a result of reduced
female aggressiveness). Female tassel-eared squirrels have been observed to solicit copulations
from subordinates (Farentinos, 1980).
After reviewing the literature, Dewsbury (1982b) concluded that male dominance was cor-
related positively with relative frequency of copulation in the majority of rodents studied,
although the correlation did not hold for all conditions. The effects of confinement are difficult
to exclude in most studies. The fact that greater reproductive success of dominant male Pero-
myscus was evident in large enclosures but not in smaller ones (Dewsbury, 1981) suggests that
in unconfined situations the expression of female preferences is likely to be more, rather than
less, effective. This might not be true, however, in the more social species. In black-tailed prairie
dog towns, where numerous males occur within a short distance, females mate primarily with
males that are members of their own coterie (Foltz and Hoogland, 1981).
Schwartz and Armitage (1980) reported that recruitment of male colony members appeared
to be largely from outside the colony in Marmota flaviventris. Armitage (1986b) concluded that
there was no evidence that female yellow-bellied marmots made choices among males. If a
harem male disappeared, females simply remained in the colony without breeding until another
male appeared and took control of the harem. It would not be surprising if replacement of males
followed this pattern in murine rodents. However, removal of males from house mouse popu-
lations produced no evidence of recruitment of mature male immigrants and mating was pre-
sumably suspended until male offspring were recruited (unpubl. personal observation).
There are few clues in the literature as to mating preferences of resident females with respect
to male offspring. Maternal presence in close confinement has not been reported to inhibit sexual
maturity of sons and presence of sons under these conditions has not been reported to inhibit
maternal estrus. Grau (1982) interpreted the high frequency of female approaches toward related
males as possibly indicative of inbreeding avoidance. However, he also observed that female
Peromyscus leucopus investigated unfamiliar male siblings but chased unfamiliar non-sibling
males, which casts doubt on the inbreeding-avoidance explanation.
Baker (1981b) carried out six experiments in which cages containing small demes were joined.
In five experiments the demes merged. Females mated with the “foreign” males in two exper-
iments, but in the other three the females mated with the “local” as long as the opportunity was
present, mating with the foreign male only when the local male had been killed. These results
seem to indicate that females favored familiar males as long as those males were able to maintain
dominant status. Cox (1984) found that female Mus from adjacent granary populations selected
the odor of their own colony over that of the neighboring colony when offered a choice in an
experimental apparatus. They also avoided the odors of males from the alien population. Heth
and Nevo (1981) reported that female mole rats (Spalax ehrenbergi) from both central and
peripheral populations also showed preference for local mates over “foreigners.”
In contrast to the abundant evidence on female preferences, there is little evidence that males
are selective. In laboratory tests, Godfrey (1958) reported that male Clethrionomy: showed
preference for females from local as opposed to more distant populations. Fleming et al. (1981)
Y
Testing RFH 57
reported that male Neotoma spent more time sniffing the urine of familiar estrous females than
that of unfamiliar estrous females.
The evidence reviewed implies that females tend to make choices, but that males are less
discriminating with respect to mates. Except in monogamous species, and to a lesser extent in
highly social species, there is little evidence of male choice beyond a generalized tendency for
males to behave aggressively toward unfamiliar conspecifics. Choice by both sexes tends to be
in favor of familiar and, therefore, more closely related mates.
All females appear to prefer mates that are familiar and are established and dominant on
home ranges. Mate choice in both sexes is restricted primarily by sedentarity, territoriality, and
social organization.
How Common Is Inbreeding?
How much inbreeding does occur in nature? Is there widespread evidence for inbreeding
depression, or of heterosis, in natural rodent populations? Is reduction of the probability of strong
inbreeding an unselected by-product of physiological or behavioral patterns that have evolved
on some other basis? Do natural populations and environments exhibit enough stability for
behavioral patterns to evolve on the basis of their contribution to inbreeding avoidance? Is the
degree of familiarity that acts as a barrier to mating in some species in the laboratory replicated
in nature? Is the loss of opportunity for altruism a significant cost when inbreeding is avoided?
Both inbreeding and outbreeding have costs and benefits and the optimal mate choice may
be the one that maximizes benefits relative to costs (Bateson, 1983; Shields, 1983). In the following
discussion it will be useful to keep in mind the distinction drawn by Moore and Ali (1984)
between strong inbreeding (coefficient of kinshiop 0.25 or more) and close inbreeding (coefficient
of kinship between 0.125 and 0.25), as well as the relation of these specific terms to the more
general concept of inbreeding as it occurs in demes of less than a few thousand individuals. It
is also worth noting that even low levels of inbreeding can have significant effects on the rate
of change in gene frequency (Breden and Wade, 1981).
The questions above are important to the evaluation of the emigrant fitness and resident fitness
hypotheses of dispersal. Avoidance of incestuous matings has frequently been advanced in support
of emigrant fitness, and is in that sense a likely basis for challenge of the RFH. However, it is
not essential to the RFH that inbreeding have no net cost. To the contrary, if inbreeding depression
does entail a net cost to the parent in an incestuous mating, parents should export young in order _
to avoid inbreeding cost. If inbreeding has a potential for costs, it also has a potential for benefits.
Inbreeding creates a favorable environment for the evolution of altruistic behaviors through kin
selection (Breden and Wade, 1981).
The proliferation of reports of presumed inbreeding avoidance obscures the fact that there
are many behaviors that could be described as inbreeding facilitation. Mates chosen at random
in a population of largely philopatric rodents might on average be no more distantly related
than second cousins. The probability of close genetic relationship between mates will be increased
if young of either sex tend to remain at the natal site; if parents in some way facilitate inheritance
of the natal site (nepotism); if “survival” habitat occurs in small, isolated patches supporting only
a few breeding pairs of individuals; if there are tendencies for relatives to behave aggressively
toward strangers but in a neutral, affiliative, or altruistic manner toward familiar individuals
such as parents or littermates; if populations are founded by a pregnant female or a pair; if there
is resistance to immigration; if there are “social fences’; or if there is a tendency for young to
emigrate in company with other members of the same litter. Inbreeding is also favored over
any time period in which habitat conditions are stable. Inbreeding could be favored by selection
if outbreeding leads to breaking up of combinations of alleles whose overlapping effects lead to
advantageous phenotypes.
It is worthwhile to examine some of these “inbreeding facilitation mechanisms” in some detail.
Parental nepotism strongly favors inbreeding. Female nepotism and the formation of matrilineal
groupings is widespread among the terrestrial sciurids (Armitage, 1986b; Hoogland, 1981; King
58 Rodent Dispersal
and Murie, 1985; Michener, 1983b; Sherman, 1980), and the sciurid model could apply to other
rodents as well. The formation of matrilines implies that the offspring of neighboring females
will be closely related and most polygynous males will mate with females that are close relatives,
if not sisters or daughters. The degree of inbreeding in such situations will be determined primarily
by male dispersal distances, and avoidance of close inbreeding would require that minimum
male dispersal distances must be greater than 1.5 female range diameters. The distance would
have to be still larger if male home ranges are larger than female ranges.
Dominance hierarchies among males tend to limit mate choice by females and increase
opportunities for matings between the dominant male and sisters or daughters. In polyestrous
species, philopatry of offspring of either sex during the breeding season creates opportunities for
parent-offspring and sibling matings. In seasonal breeders cohesiveness among members of fam-
ilies over the non-breeding season increases the possibility of parent-offspring matings where
parents survive to breed again, and of sibling matings if parents are no longer available. Among
temperate zone mice and voles, close relatives often overwinter together (King, 1983; Mihok,
1979). Some non-siblings might join overwintering groups (Madison, 1984; Wolff, 1980; Wolff
and Lidicker, 1980), but there seems to be no evidence that closely related individuals sponta-
neously leave or are forced from such groups.
Habitat patchiness accentuates behavioral tendencies toward inbreeding. This is especially
likely if patches are well-separated and small relative to territory size. Pairs of individuals taken
at random are more closely related to each other in small populations than in large populations
(Partridge, 1983). The point can be appreciated easily in a small non-rodent, Ochotona. Smith
and Ivins (1983) found that well-defined small patches of scree habitat were associated with
philopatry and incestuous mating. Although boundaries are often less easily identified in many
rodent habitats, I suspect they are similarly discrete from the point of view of their occupants.
Exclusive breeding structure is apparent in some small commensal Mus populations (Anderson,
1964, 1965; Petras, 1967a) in which habitat boundaries are readily discernible. Goundie and
Vessey (1986) observed little movement in or out of woodlots inhabited by Peromyscus leucopus,
concluding that the short dispersal distances observed indicated that close inbreeding was prob-
able.
Even in superficially more homogeneous environments, patchiness might be sufficient to pro-
mote inbreeding, at least when regional density is low. Bowen (1982) reported that in Microtus
californicus living in continuous grassland, electromorphs from blood samples collected at first
capture of voles on four nearby quadrats revealed that genetic heterogeneity (measured as the
F statistic) was high at low density. Heterogeneity appeared to decrease as density increased
over the single breeding season of the study. As Bowen’s comparisons were between grids, rather
than habitat patches, however, it is not clear whether the decrease in heterogeneity was due to
a decline in inbreeding as Bowen believed, or simply the result of the filling in of the interstices
between permanently occupied sites by settlers as the breeding season progressed. The latter
interpretation is in keeping with the results obtained by Pearson (1960).
As development and application of statistical and electrophoretic techniques have proceeded,
it has become possible to make increasingly sophisticated analyses of genetic structure. Studies
designed to detect departure from random mating have produced mixed results. Evidence of
small effective population size, inbreeding, and genetic drift has been adduced in house mice
(Anderson, 1964, 1965; Petras, 1967a, 1967b; Selander, 1970a, 1970b; Selander et al., 1969b;
Singleton, 1985), deermice (Rasmussen, 1964), voles (Nygren, 1980), pocket gophers (Patton and
Feder, 1981; Selander et al., 1974), prairie dogs (Chesser, 1983), and marmots (Schwartz and
Armitage, 1981). Following studies of house mice in farm buildings, Petras (1967a, 1967c)
estimated inbreeding coefficients of 0.06 to 0.30 on the basis of biochemical polymorphisms and
0.18 on the basis of an agouti coat-color locus. He also observed heterozygote deficiencies.
Singleton (1985), in a study of house mice inhabiting haystacks, reported that genotypic fre-
quencies at the GPI-1 locus matched Hardy-Weinberg predictions for random mating, but that
Testing RFH 59
there was a deficiency of heterozygotes at the Hbb locus. Nygren (1980) found a general excess
of homozygotes in Microtus agrestis over the course of a fluctuation in density. Patton and Feder
(1981) reported high positive F,, values, indicating heterozygote deficiencies, for most of 11 loci
examined in an undisturbed population of Thomomys bottae. Following removal and recolo-
nization, F,, values were largely negative or non-significant, suggesting that inbreeding did not
occur during recolonization. Despite the evidence for inbreeding in the undisturbed population,
Patton (1985) has concluded that microgeographic variation in pocket gophers is due primarily
to founder effects, rather than to inbreeding and restriction of gene flow. Parallel conclusions
have been advanced for mole rats (Spalax) by Nevo et al. (1982).
Heterozygote deficiencies might or might not indicate inbreeding, depending on selective
pressures. Most studies have dealt with one or a few loci, and single-locus studies might be poor
indicators of breeding structure because it is difficult to show that a given locus would not be
affected by strong selection. Experimental matings, designed to compare the fitness of intra-
population and inter-population matings, might be an effective alternative approach tv detection
of inbreeding. Comparison of litter size in within-population and between-population matings
of granary house mice showed evidence of heterosis in the latter (larger mean litter size), implying
that significant inbreeding was occurring within the studied populations (Anderson, unpublished).
Modeling studies designed to test possible explanations for the persistence of mutant alleles in
house mice have supported empirical evidence of inbreeding in that species (Lewontin, 1962;
Lewontin and Dunn, 1960). Maynard Smith and Stenseth (1978) suggested, on the basis of
modeling, that inbreeding could be responsible for the stability of female-biased sex ratios in
litters of some microtines. They also suggested that a high degree of inbreeding might characterize
fluctuating microtine populations during periods of low density.
Although sufficiently detailed studies of dispersal are still scanty, some do suggest that in-
breeding might be common. Wolff and Durr (1986) found that nearly one third of overwintered,
fall-born Peromyscus leucopus females bred within the range of a possible father. In P. manicu-
latus a third of the young also overwintered and bred within their natal home ranges. Jones
(1984) reported that at least one male Dipodomys spectabilis shared a mound with his mother
in his first breeding season.
Other investigations have provided evidence for random mating and/or outbreeding tenden-
cies. Genetic evidence for significant gene flow has been found in several house mouse populations.
Such evidence has been associated with disturbance due to agricultural practices, experimental
manipulation, or both (Baker, 1981b; Justice, 1962; Myers, 1974), or severe overwinter mortality
(Berry and Jakobson, 1974, 1975). Petras (1967a) postulated that Mus populations on farms might
fall into two categories, those that were permanent and those that were relatively ephemeral.
In more ephemeral populations the constant turnover of individuals eliminated any opportunity
for inbreeding. Foltz (1981a) found no evidence of a departure from panmixia in Peromyscus
polionotus and his re-evaluation of data from other studies of Peromyscus casts doubt on previous
analyses suggesting inbreeding in that genus. Foltz and Hoogland (1983) found that all of four
polymorphic loci examined in a colony of black-tailed prairie dogs showed an excess of hetero-
zygotes, a possible result of negative assortative mating. Pedigree analysis supported this indication
of low levels of inbreeding and Foltz and Hoogland concluded that behavioral observations of
these ground squirrels suggested that inbreeding among close relatives would be rare enough to
make inbreeding coefficients very low. However, variability across the electrophoretically ana-
lyzed loci suggested other explanations, including selection, for the excess of heterozygotes. Foltz
and Hoogland (1983) emphasized that it was difficult to attribute heterozygote excess specifically
to any of the several possible causes.
Other studies have demonstrated that the laboratory data on inbreeding depression should not
be casually extrapolated to the field situation. Davis (1984) manipulated relatedness in Sper-
mophilus richardsonii on two areas so that the coefficient of relatedness was much less than 0.5
on one, and close to 0.5 (between 0.25 and 0.5) on the other. In the more inbred group there
60 Rodent Dispersal
was evidence that inbreeding and close relatedness conferred benefits: above-ground time spent
feeding was greater; vigilance was less; sharing of core areas among neighbors was greater;
interactions leading to chasing and flight were reduced; and breeding success was increased.
Overall, we are poorly informed as to the actual extent of inbreeding in the majority of
commonly studied rodent species. At the present time it is not unreasonable to predict that
close (near relative) inbreeding is the normal state of affairs in many populations. If this were
the case, deleterious recessive alleles would be maintained at a relatively low frequency because
of their frequent exposure to selection. Occasional or even frequent close inbreeding might then
not be very costly. If laboratory evidence alone is relied on, the logic in support of the notion
that inbreeding should be avoided seems clear. The theoretical and experimental evidence as to
the possible cost of inbreeding notwithstanding, it is apparent that if populations maintain social
stability, matings among close relatives are probable. Further studies are needed to address
directly the question of degree of inbreeding, amount of gene flow, frequency of founder effects,
and genetic structuring under a variety of conditions. The evidence that gene flow in house mice
is promoted in environments where there is frequent disturbance of population structure raises
two important questions applicable to many species. Which populations are most representative,
stable inbreeding populations or high-turnover outbreeding populations? Is frequent disturbance
so sufficient at preventing close inbreeding that other barriers are unlikely to have selective
value?
Barriers to Inbreeding
Close inbreeding can be prevented by separation of near relatives in time or space, or by
behavioral or physiological restraints. Selection against inbreeding has been an attractive expla-
nation for various behavioral and physiological phenomena. Sherman and Holmes (1985), for
example, suggested that greater development of kin recognition in the more nepotistic sex
(females) might be due to its potential contribution to inbreeding avoidance.
The attractiveness of such explanations should not be allowed to obscure the fact that the
opportunity for strong inbreeding might be limited by factors that are difficult to relate to
inbreeding depression. Seasonal breeding, for example, might influence the probability that
matings will be incestuous. Mortality over the non-breeding season can significantly reduce the
opportunity for parent-offspring or sibling matings, and relaxation of territorial defense during
the non-breeding season might eliminate behavioral barriers to immigration and create oppor-
tunities for outbreeding when reproduction is resumed. Predation on Microtus pennsylvanicus
over the winter months, combined with relaxation of aggressive behaviors and a requirement of
sufficient group size to make huddling an effective protection against low temperatures, leads
to admission of strangers into overwintering families (Madison, 1984). Similar tendencies for
development of aggregations of unrelated individuals during the non-breeding season have been
reported by Myllymaki (1977a), Wolff (1980), and Wolff and Lidicker (1980, 1981). Seasonal
changes in habitat could have similar consequences. Mihok (1984) noted massive immigration
of overwintered M. pennsylvanicus at the start of the breeding season, associated with a seasonal
shift from wintering habitat (forest) to spring, summer, and fall habitat (grasslands). As visualized
by Shields (1983), the resulting “injection” of outbreeding might be an effective counter to the
decay of heterozygosis in otherwise inbreeding populations. Tropical dry seasons might have
effects similar to those of high-latitude winters. In the capybara, for example, large aggregations
form near water in the dry season (Schaller and Crawshaw, 1981).
Hoogland (1982) attributed the rarity of parent-offspring and sibling matings in Cynomys
ludovicianus to emigration of young males, death or emigration of adult males before philopatric
daughters reach breeding age (males that survived the first year of life lived only an additional
3-4 years, whereas females lived an additional 4-5 years), failure of philopatric daughters to
come into breeding condition when the father remained in the natal coterie, and behavioral
avoidance of closely related males by estrous females. Upon further scrutiny, however, Hoogland’s
data do not appear to support the hypothesis that there are specific adaptations for inbreeding
Testing RFH 61
avoidance. The first of the four mechanisms (male emigration) eliminated the possibility for
inbreeding in 90.4% of the instances studied. As Greenwood (1983) emphasized, it is difficult to
disentangle cause and effect with respect to the role of emigration as a barrier to inbreeding. If
male emigration evolved from other causes, as postulated by the RFH, it does not support
Hoogland’s (1982) case for behavioral avoidance of inbreeding. The observed deaths of harem
males also can be explained without evoking selection against inbreeding.
Hoogland’s data show that although a significantly lower proportion (2/26) of yearling females
copulated when the paternal male was present in the coterie, only a minority (13/37) of yearling
females copulated when the paternal male was not present. This suggests that, as with male
emigration, absence of estrus in a yearling female might be due to factors other than incest
avoidance. If cause and effect interpretation is suspended with respect to male emigration and
delayed reproduction of yearling females, Hoogland’s argument for behavioral avoidance then
must rest primarily on the cases of seven females that had an opportunity to copulate with a
father, son, or sibling. Two did so, but copulated with a less closely related male as well, and a
third did so in 2 of 3 years. Three of the remaining four copulated exclusively with the less
closely related of two available males; the other copulated in a neighboring coterie and subse-
quently returned home. There were, therefore, only three instances in which females were known
to have mated exclusively with partners less related than immediate family. As there were also
three females that did mate with closely related males, and one for which the data are apparently
inconclusive, a strong argument cannot be made for inbreeding avoidance.
In yellow-bellied marmots, as in prairie dogs, the major obstacles to inbreeding appear to be
the emigration of young males and the death of older males before philopatric daughters mature
(Schwartz and Armitage, 1980). The same conclusion applies to other ground squirrels (Dobson,
1979, 1981; Michener, 1980, 1983b; Michener and Michener, 1977; Sherman, 1980). In all of
these monestrous species, parental mortality prior to sexual maturity of offspring could be the
major obstacle to parent-offspring matings.
Inbreeding might be restricted if inhibition of sexual development in juveniles results from
exposure to pheromones produced by sexually active adults of the same sex. Confinement of
young with sexually active parents or siblings under laboratory conditions can inhibit sexual
maturity of young mice or voles (Batzli et al., 1977; Haigh, 1983b; McGuire and Getz, 1981;
Rissman et al., 1984; Terman, 1980). Schadler (1983) found that presence of a brother sequestered
behind wire mesh inhibited matings between female pine voles and unrelated conspecific males
(Schadler did not, however, determine whether the presence of an unrelated male was similarly
inhibitory). Inhibitory effects such as these are not demonstrable in some species (Batzli et al.,
1977; Facemire and Batzli, 1983; Wilson, 1982) and might not be widespread among rodents.
These phenomena might be dependent on close, continuous confinement; Milligan (1980) re-
viewed the data and concluded that ideas about biological significance of almost all laboratory-
derived phenomena of this type were speculative. Two-year-old female yellow-bellied marmots
are less likely to breed when older females are present in the colony (Armitage, 1986b); this
would reduce chances of their mating with their fathers. Such behavior could have evolved
through selection for mechanisms by which maternal females limit competition and thereby
maximize their own production of offspring at the expense of the reproductive success of their
daughters. Inhibition in young female voles observed by Bujalska (1970, 1971, 1973) also seems
to be related to regulation of competition among females, rather than to inbreeding avoidance.
The response of non-adults might then be viewed as a complementary strategy, effective in
delaying emigration (Rissman et al., 1984) and facilitating philopatry. Direct inhibition of mat-
uration of female young by adult female pheromones seems most readily explained in terms of
female competition, nepotism, and retention of female young as helpers. Maturity delays asso-
ciated with parental pheromones need not be explicable solely as barriers to incest.
Inadequate stimulation is the alternative to direct pheromonal inhibition of juvenile devel-
opment. Lendrem (1985) compared age at first estrus of immature female Mus musculus exposed
to soiled bedding from the cages of more closely and less closely related males. Females exposed
62 Rodent Dispersal
to bedding from the cages of male cousins matured at a significantly earlier age than those
exposed to bedding from the cages of fathers or uncles. It appeared that the odors of more
distantly related males accelerated puberty.
The most thorough investigations of a behavioral/physiological mechanism with the potential
to reduce the frequency of inbreeding were by Getz, Carter, and co-workers on Microtus
ochrogaster. This species is a special case because of tendencies to monogamy and to postnatal
investment by the father. Up to 50% of breeding units in the field are monogamous (Getz and
Hofmann, 1986); in the laboratory males provide paternal care in the nest (Thomas and Birney,
1979). Mechanisms inhibiting mating by other than the parental pair while a family group
remains together are evident in males as well. Sons do not attempt to mate with their mothers
in postpartum estrus, and young males maintained in family groups show reduced tendency to
mount when placed in a pen with an unfamiliar estrous female (Carter and Getz, 1985).
As in other microtines, ovulation must be induced by copulation in M. ochrogaster. Females
copulate only when in estrus. To achieve her initial estrus, a pubescent female must be sexually
activated by exposure to a male pheromone. In confinement, at least, young females do not make
naso-genital investigations of familiar males. Therefore, they are not exposed to male pheromones
and remain sexually quiescent (Gavish et al., 1983, 1984; Getz et al., 1983; McGuire and Getz,
1981). If parents and offspring share a nest in nature, virgin females probably are unlikely to
be activated by their fathers or brothers and thus apparently are unlikely to mate for the first
time with a near relative. Because a pair-bond is formed at first mating, females are also unlikely
to mate incestuously in later matings.
The obstacle to inbreeding in M. ochrogaster is familiarity, not relatedness. If urine from a
familiar male is placed on the nose of an inactive female, activation and fertile matings are
induced. If familiar males are removed for 8 days and then returned, naso-genital investigation
occurs and activation of females and mating follow (Getz and Carter, 1980; McGuire and Getz,
1981). This opens the question as to whether inbreeding avoidance is the entire, or even the
correct, interpretation. Some of the laboratory data also raise questions as to how activation can
occur in nature if the system operates as it does in confinement. The activation process observed
in the laboratory requires that a young female remain with an unfamiliar male for 24 to 48 h.
However, both pair-bonded males and sexually experienced but unbonded males are aggressive
toward unfamiliar virgin females (Gavish et al., 1983). If an activated female is returned to the
family group in the laboratory, activation could be suppressed by maternal pheromones. Con-
finement of two virgin females together prevents sexual activation of one or both (Carter and
Getz, 1985). In the field, most females that survive to maturity are philopatric (Getz and Hofmann,
1986; Getz et al., 1987). It seems, therefore, that explanations other than incest avoidance should
be considered. Young assist in rearing younger siblings in the laboratory (Gruder-Adams and
Getz, 1985). Inhibition of female maturation in M. ochrogaster might function to retain female
young in the nest as helpers or to limit female competition or both. There is a good case for
expecting that familiarity will make father-daughter and sibling matings unlikely, but alternative
explanations for the process by which it is achieved should be sought. Parental strategies serving
to control emigration and reproduction of offspring might be revealed.
Familiarity reduces the probability of within-litter incest in some other voles as well. Boyd
and Blaustein (1985) reported that although sibling and non-sibling pairs produced litters of
equivalent size and viability, young Microtus canicaudus that had been reared together to
maturity produced fewer litters than those that were unfamiliar when paired. Separation for 5
or 12 days did not reduce reluctance to mate. It thus appears that in nature littermates would
be less likely to mate than non-littermates. Despite the absence of detectable inbreeding depres-
sion, Boyd and Blaustein (1985) characterized the disinclination to mate as an inbreeding avoid-
ance mechanism and speculated that inbreeding might be characteristic at low density because
non-littermates might be unavailable.
The evidence for barriers to inbreeding in other rodents is similarly tantalizing but questionable.
Dewsbury (1982c) cross-fostered Peromyscus eremicus and P. maniculatus prior to eye opening,
and paired siblings and non-siblings directly and after 4, 8, or 24 days separation. Although fewer
Testing RFH 63
sibling pairs produced litters than non-sibling pairs in P. maniculatus, the difference in number
of successful pairs was not significant. The non-sibling pairs produced significantly more litters,
but within litters there was no difference in the number of pups born or weaned, or in the
percentage weaned. In P. eremicus, non-sibling pairs were significantly more likely to produce
litters than were siblings or pseudo-siblings (fostered). Non-siblings produced more young at
birth, more weaned, and a higher percentage weaned. The pseudo-sibling pairs (born to different
females but cross-fostered) had the highest percentage of pups weaned, but mean litter size was
significantly higher in matings between siblings. Separation of sibling P. eremicus for 4 to 8 days
did not eliminate differences between sibling and non-sibling pairs, but there was little difference
when pairs were mated after 24 days separation.
Skryja (1978) found no evidence of either delayed matings or infertility in father-daughter
pairings of P. eremicus, but confinement of young females with their mothers and fathers was
more inhibitory to daughters than was confinement with the father alone. If the maternal female
was absent there was no difference in age at first reproduction between females caged with their
fathers and those caged with unfamiliar males. Daughters had no inhibitory effects on maternal
reproduction.
If it is assumed that mechanisms for inbreeding avoidance have been selected, it is necessary
to explain why kin recognition and reproductive inhibition appear to be sexually asymmetrical.
Lack of stimulation that is based on familiarity is unlikely to be effective in preventing father-
daughter matings where the father does not inhabit the nest with the young (most rodent species).
The higher probability that male offspring will emigrate and the longer dispersal distance of
those that do so appear to be the only restraints limiting strong or close inbreeding on the part
of males.
Kin recognition and other male behaviors that relate to inbreeding or altruism have been little
studied. D’Udine and Alleva (1983), reviewing the work of Yamazaki et al. (1976), concluded
that male Mus could exhibit either positive or negative choice of female genotypes at the H-2
locus and suggested that males might select for an optimal level of outbreeding. D’Udine and
Partridge (1981) found that cross-fostered males showed a preference for siblings whereas males
reared by their own mothers preferred non-siblings.
The inbreeding avoidance explanation of direct pheromonal inhibition can be questioned on
the grounds that the mechanisms are intrasexual, rather than intersexual. In Peromyscus manicu-
latus, for example, sexual maturation of young males is inhibited by the pheromones released
by adult males, but not by those of adult females (Lawton and Whitsett, 1979). In conjunction
with pheromonal cueing of maturation of young of the opposite sex, pheromonal inhibition of
maturation of young of the same sex may facilitate parent-offspring mating.
Pheromonal cueing has been studied most intensively in the house mouse. Maternal pheromones
tend to accelerate maturity in male offspring, and paternal pheromones tend to accelerate
maturity in female offspring (Milligan, 1980). This is likely to be the pattern for most rodents.
The relationships are consistent with the concept of intrasexual competition, but not with that of
inbreeding avoidance. Inbreeding facilitation seems to have been largely overlooked in the
enthusiastic search for inbreeding avoidance.
Inbreeding avoidance might be a seductive explanation for interactions that have subtle and
more complex foundations. The operation of pheromonal and behavioral systems that have effects
on the probability of inbreeding needs to be carefully evaluated under field conditions before
conclusions are drawn as to evolutionary significance. More elaborate and more natural exper-
iments are needed before it can be established clearly that the various maturity-delay phenomena
observable under laboratory conditions occur in nature, or function there as barriers to inbreeding.
Selection on the basis of the cost of inbreeding has a strong basis in mathematical prediction,
but a weak one in data from natural populations. In many cases, inbreeding depression might
be temporary because deleterious recessives are rapidly eliminated (Templeton and Read, 1984).
Behaviorally, inbreeding can be limited by expulsion of offspring, voluntary emigration of
offspring or parents, active avoidance, active preference for unrelated mates, failure to discrim-
inate against unfamiliar individuals, sex differential in export of offspring, or sex differential in
64 Rodent Dispersal
site tenacity of parents or offspring. Physiologically, delayed or suppressed sexual maturation of
young in the presence of adults or littermates can make inbreeding unlikely. Avoidance of
inbreeding depression presents itself as an attractive evolutionary explanation, but none of the
behavioral and physiological phenomena described needs to function exclusively, or even pri-
marily, as a deterrent to inbreeding. The lack of evidence for male choice is partly due to lack
of investigation, but unselective mating by males is in accord with the prediction that at least
in polygynous species males would have little to gain by selectivity.
I suspect that in nature more opportunities for inbreeding are eliminated by mortality, seasonal
changes in behavior, and environmental instability than by inbreeding avoidance. Jones (1984)
concluded that high mortality was probably the major factor limiting development of groups of
closely related Dipodomys spectabilis. Patton (1985) has also concluded that low individual
survivorship is the dominant force for outbreeding in Thomomys. Selection for avoidance of
inbreeding is unlikely where there is little opportunity for inbred matings due to frequent habitat
disruption, high turnover rates of males due to mortality, or male emigration. Selection against
inbreeding is also unlikely if its costs are low relative to the high costs of emigration. Where
selection against inbreeding does exist, it might operate primarily against parent-offspring and
sibling matings and have little effect on mating at other levels. Because rodents can occupy
habitat patches of small size, selection for local adaptation and coadaptation, as defined by
Templeton et al. (1986), could be as important as selection against inbreeding. I think it premature
to conclude, as Sherman and Holmes (1985) have done, that kin recognition exists largely because
it contributes to avoidance of inbreeding depression.
Male Competition for Copulations
Variation in male mating success is likely to be high in most rodent populations because mating
systems are polygynous (Kleiman, 1977) and operational sex ratios are biased toward females
(e.g., Jannett, 1980; Redfield et al., 1978a; Schaller and Crawshaw, 1981). As expected, intrasexual
aggression is correlated with sexual maturity in males. Sexually active male rodents of most
species are mutually antagonistic if placed in arena situations, although some species rely more
on avoidance and less on combat (Colvin, 1973; Cranford and Derting, 1983). Aggressiveness in
males provides strong circumstantial support for the hypothesis that males compete for copu-
lations.
Male aggression appears with the onset of sexual activity both seasonally and ontogenetically.
Thereafter, aggression is maintained at a more or less constant plateau, declining as the end of
the breeding season approaches. If there is variation during this period it can occur in response
to such stimuli as the presence of estrous females or challenges from other males or both.
The association of male aggression with sexual maturity and with the breeding season in nature
is well documented (Boonstra, 1978; Fairbairn, 1977a, 1978a; Healey, 1967; Llewellyn, 1980;
Perrin, 1979; Sadleir, 1965; Turner and Iverson, 1973). Laboratory studies have shown that male
aggression is correlated with high levels of circulating steroids. In Clethrionomys glareolus, for
example, Gipps (1983, 1984) demonstrated that male fighting and wounding were dependent
on the level of circulating androgens, and that prepubertal castration reduced the tendency to
fight.
Aggression is also positively associated with the opportunity to copulate. Aggression among
sexually mature male Peromyscus is enhanced by the presence of females (Dewsbury, 1984;
Terman, 1984). The introduction of a female into an all-male group of Mus induced aggressive
interactions among the formerly compatible males (Petrusewicz, 1963). The probability of ag-
gressive behavior in male Microtus californicus increased with proximity to a caged estrous
female (Ostfeld, 1985b), and reproductively active male voles have been observed to be mutually
aggressive in the field in the vicinity of estrous females (Webster and Brooks, 1981). Removal
of female M. pennsylvanicus from an experimental plot increased persistence (i.e., survivorship)
of adult males on the plot during the breeding season (Boonstra and Rodd, 1983; Rodd and
Boonstra, 1984). However, removal of overwintered female Clethrionomys rutilus after weaning
Testing RFH 65
of the first litter did not affect persistence of overwintered males (Gilbert et al., 1986). Aggres-
siveness in male rodents is directed primarily toward individuals that could compete for matings:
immature males can be tolerated where mature males would be attacked (Gipps, 1984). Pher-
omones produced by adult males have been shown to suppress sexual development of young
males under laboratory confinement (Bediz and Whitsett, 1979; Lawton and Whitsett, 1979;
Vandenbergh, 1971). Male chipmunks congregated in the home ranges of females in estrus
(Yahner, 1978), and radio-collared male meadow voles have also been observed to move into
the home ranges of estrous females (Madison, 1980a). Males are known to increase the size of
their ranges with the onset of breeding (Korn, 1986; Madison, 1985; Randolph, 1977). Ostfeld
et al. (1985) reported that the dispersion of sexually active male Microtus californicus was
affected more strongly by competition for access to females than by competition for access to
food.
Male home ranges are typically larger than those of females (Bondrup-Nielsen and Karlsson,
1985; Mazurkiewicz, 1981; Ostfeld, 1986; Scheibe, 1984), despite the higher energy requirements
of gestating and lactating females. Ostfeld (1986) found that supplemental food caused a reduction
in the size of home ranges in females but had no effect on those of males. During the mating
season, male Spermophilus richardsonii moved over greater distances and engaged in more fights
than females (Michener, 1983a). Male ranges are more likely to overlap than are those of females
(Madison, 1985). Lidicker (1985b) stated that recapture frequencies of male M. californicus
differed from those of females in that the latter were correlated with habitat quality, whereas
male recapture frequencies were not. These intersexual differences imply that female availability,
rather than nutritional resources, might be the reference system for use of space by males.
Male maturity and inter-male competition typically precede the seasonal availability of re-
ceptive females. In most obligately-hibernating ground squirrels, males emerge and establish
hierarchical social relationships through agonistic encounters prior to emergence of females
(Armitage, 1986b; Michener, 1983a; Sherman, 1981; Yahner, 1978). Overwintered male voles
are more aggressive, have larger home ranges, and survive longer than male young of the year
(Turner and Iverson, 1973). Dominant and early-emerging males are more successful at mating
than subordinates or those that emerge later (Michener, 1983a). Mating success of male S.
tridecemlineatus is correlated with both age and weight (Schwagmeyer and Brown, 1983).
Dobson (1983) reported that male S. beecheyi appeared to guard receptive females. Armitage
(1986b) has shown that fitness of male marmots increases with harem size.
Male aggressiveness often declines or ceases as soon as receptive females are no longer available.
Most ground squirrel species either follow similar patterns to those described or differ in ways
that are consistent with intrasexual selection (Michener, 1984).
If successful competition for copulations depends on a claim to space, male territoriality
(defined here as scent marking, aggression, or other behavior leading to occupancy of space to
the exclusion of some category of conspecifics) is most likely to be expressed in the breeding
season. Adult males have been found to occupy home ranges that overlap those of females, but
not those of other adult males in marmots (Armitage, 1974), California ground squirrels (Dobson,
1983), house mice (Fitzgerald et al., 1981), woodrats (MacMillen, 1964), pocket mice (MacMillen,
1964), and voles (Jannett, 1980, 1981a; Wolff, 1980).
Overlapping ranges of resident males have been reported in many species, including some of
those listed above (Daly and Daly, 1975; MacMillen, 1964; Oakshott, 1974; O'Farrell, 1980;
Webster and Brooks, 1981). If males compete intensely, why do male home ranges sometimes
overlap? Boonstra and Rodd (1983) postulated that breeding male M. pennsylvanicus formed
dominance hierarchies among individuals with overlapping ranges. Ostfeld (1985a) has argued
that male territoriality is dependent on female strategy, and that male behavior should be
territorial when female ranges are mutually overlapping, and non-territorial when female ranges
are mutually exclusive.
Perhaps the view that males are not territorial when male home ranges overlap is simplistic
and misleading. Territoriality is evident in its simplest and most generally accepted form when
66 Rodent Dispersal
male residents occupy space to the exclusion of all other breeding males. Definition of male use
of space as non-territorial wherever there is overlap in ranges of breeding males (Lidicker, 1980;
Madison, 1980a, 1980b, 1985; Wolff, 1980) overlooks the possibility that there might be advantages
to males in various forms of cooperative or communal defense of space. The possibility that
overlap might indicate that males are cooperating in defense of territory, and therefore of mating
rights, needs investigation. Cooperative defense of an area by equals, relatives, or members of
a dominance hierarchy may exclude neighbors or transients. Communal territories are easily
defined in Microtus pinetorum (Cranford and Derting, 1983; FitzGerald and Madison, 1983),
suggesting that they may be present in other less obvious forms in those microtines where male
ranges overlap. Stable groupings of 2 to 4 breeding males, suggesting inter-group territoriality,
have been described in Clethrionomys rufocanus (Viitala and Hoffmeyer, 1985). In a comparative
study of M. pennsylvanicus and M. pinetorum, Cranford and Derting (1983) concluded that
males of the former species maintained individual distance through mutual avoidance. The
question of whether overlapping ranges formed a continuum or represented mating “communes”
was not addressed, and the degree of relatedness of overlapping males was not considered. The
difference between those situations where male ranges overlap and those where they do not may
relate to habitat characteristics and the effectiveness with which space can be defended by
fighting, chasing, and patrolling, or by scent marking or other means of display. It may also
depend on the degree to which other males threaten copulatory success.
Scent marking might play an important role in assertion of male mating rights. Jones and
Nowell (1974) showed that urine of male Mus contained an aversive substance that caused
subordinate males to avoid scent marked areas. Wuensch (1982) found that in the field, traps
scented by wild male Mus dominant in laboratory encounters were more likely to be visited by
resident males than were those scented by males that had been subordinate in the laboratory.
This might follow if the presence of a dominant male is more likely to threaten reproductive
success, and thus be more worthy of investigation by a resident than the presence of a subordinate.
Scent marking could serve as an alternative to combat among adult males, or to damaging attacks
by males on their offspring.
Outside of confinement, fighting may be less common and wounding more superficial than
in staged encounters in the laboratory. Schaller and Crawshaw (1981) noted that pursuing male
capybaras did not appear to make any effort to close the gap between themselves and intruding
males they chased. Nevertheless, wounds (mostly on the rump and shoulders) did accumulate
over the breeding season and some were fatal.
Competition for copulations might not have spatial reference points in all species. Observing
inter-male competition for copulations in an unconfined population of Spermophilus tridecem-
lineatus, Schwagmeyer and Brown (1983) saw no site-specific dominance. Differences among
species might be associated with habitat differences, mating systems, whether or not estrus is
male-induced, relatedness of the animals studied, or study methods.
Male territorial behavior has been repeatedly implicated as a determinant of density of breeding
males (Fairbairn, 1977a; Myllymaki, 1977a; Redfield et al., 1978a, 1978b; Wolff, 1980), and
emigration of overwintered males typically shows a peak at the start of spring breeding activity
(Boonstra and Rodd, 1983; Fairbairn, 1977a; Perrin, 1979). Myllymaki (1977a) attributed emi-
gration of spring-born males to the aggressiveness of overwintered males. In boreal populations
of M. pennsylvanicus, males enhanced their probabilities of reproductive success to a much
greater extent by early establishment in summer habitat than did females (Mihok, 1984). Mihok
et al. (1985b) found that as males came into reproductive condition, there was a high rate of
turnover during which most of the fall residents were displaced.
Boonstra and Rodd (1983) systematically tested the hypothesis that male competition for
copulations was direct, rather than through territorial claims, in M. pennsylvanicus. Removal
of females caused a reduction in male density; removal of males led to an increase in male
density. They concluded that resident breeding males restricted recruitment of breeding males
when breeding females were present. Armitage (1986b) implied that male territoriality in mar-
Testing RFH 67
mots and ground squirrels is oriented primarily toward assertion of exclusive access to females.
A male might defend a colony area containing the burrows of females, or defend a burrow near,
but not among, those of the females. Barash (1981) explored a series of predictions based on the
assumption that male marmots competed for copulations. He found, as predicted, that: 1) males
made probes outside of the colony area (“gallivants”) more than did females; 2) gallivanting
males were invariably driven from neighboring colonies if they encountered the resident male;
3) if the resident male had been removed, gallivanting males copulated with the resident females;
4) resident males attended females more closely during the breeding season and when threatened
with cuckoldry by intruders; 5) group-living (harem) males maintained closer watch on females
than-did monogamous males; and 6) males cohabiting with fertile females guarded the females
more than did males with infertile females.
Davis and Murie (1985) suggested that competition among male ground squirrels may include
both pre-copulatory competition and post-copulatory mate guarding, both of which reduce the
incidence of multiple matings. Male Microtus with overlapping ranges concentrate in the ter-
ritories of estrous females (Madison, 1980a; Webster and Brooks, 1981).
Competitive mating chases have been described for Microcavia (Rood, 1970), Microtus (Web-
ster and Brooks, 1981), Tamias (Yahner, 1978), and Clethrionomys (Kalela, 1957; Viitala, 1977).
Social dominance has been shown to correlate with breeding success of males under various
experimental regimes (DeFries and McClearn, 1970, 1972; Dewsbury, 1984; Lloyd and Christian,
1969; Reimer and Petras, 1967; Singleton and Hay, 1983). Social dominance under field conditions
has been associated with mating success in Clethrionomys (Kawata, 1985b; Mihok, 1981), Sper-
mophilus (Schwagmeyer and Brown, 1983), and Tamias (Yahner, 1978). Yahner found that as
the number of competing male chipmunks increased, the ability of the dominant male to
monopolize copulations was eventually eroded. The dominance/success relationship has been
questioned on the basis of laboratory experiments with wild and domestic strains of Rattus
norvegicus (Barnett, 1958; Dewsbury and Hartung, 1980; Price, 1980).
It is generally assumed that competition among males results in high variance in male success.
There are few direct measurements of this in nature, but Sheridan and Tamarin (1986) obtained
results suggesting that, at least among established resident males, success was fairly uniform.
Among 28 cases where paternity could be assigned in M. pennsylvanicus, 82% of the males
fathered only one litter and the remaining 18% fathered only two. If these preliminary results
can be extended to rodents in general, high variance in male reproductive success may be less
common than previously believed.
Exposure of a recently impregnated female to an unfamiliar male under conditions of con-
finement might block pregnancy and induce estrus (Bruce, 1959; Dewsbury, 1982a; Heske and
Nelson, 1984; Mallory and Clulow, 1977; Schadler, 1981; Stehn and Jannett, 1981; Stehn and
Richmond, 1975), and introduction of an unfamiliar male into a cage containing a female and
her newborn litter can lead to infanticide by the male (Mallory and Brooks, 1978). Both phe-
nomena have been viewed as mechanisms that have evolved through male competition for
reproduction (Mallory and Brooks, 1980; Schwagmeyer, 1979). Neither phenomenon has been
convincingly demonstrated in the field, in the absence of confinement, and Milligan (1980) has
speculated that the pregnancy-block effect might simply be a derailing of the system for main-
taining prolactin secretion in early pregnancy and thus a laboratory artifact. Boonstra (1980) has
concluded that there is no evidence that male infanticide increases with population density, or
is frequent enough to be of demographic significance.
There are a few reports in which male competition did not seem to be clearly oriented toward
access to females. Huck and Banks (1982b) observed dominant male lemmings ignoring receptive
females in order to seek out and attack subordinate males. Evans and Dewsbury (1978) concluded
on the basis of arena experiments with two males and a receptive female Microtus ochrogaster
that there was no justification for believing that males fought over females or that dominance
conferred a copulatory advantage. Dewsbury (1982b) later revised this conclusion somewhat in
a more wide-ranging review. Because the confined arena environment in laboratory studies often
68 Rodent Dispersal
distorts behavior and obscures interpretation (Anderson, 1961; Calhoun, 1962b; Dienske, 1979;
McClintock, 1983), the few available observations fail to discredit the view that males compete
for copulations. This conclusion appears to be as well established as it is possible for a biological
generalization to be, despite the cautions expressed by Dewsbury (1981, 1982b) and Evans and
Dewsbury (1978).
Resident Male Behavior Toward Offspring
If males are to behave paternally, they must be able to distinguish between their own offspring
and those sired by others. The fact that fertilization is internal and is separated from the initial
appearance of the young by a long interval of gestation makes it difficult for male mammals to
be certain of paternity and, as pointed out by Elwood (1983), favors abandonment of females
in search of further copulations once a mating has been achieved.
We are largely ignorant of paternal behavior in rodents; Kleiman and Malcolm (1981) were
able to cite observations on only 36 species. Elwood (1983) cited observations of paternal care
of offspring in nine genera and 23 species. All but a few of these citations referred to studies in
which paternal proximity to young was enforced by confinement. Observations of paternal care
outside of the laboratory are almost non-existent (Elwood, 1983). As far as the few field obser-
vations go, most male rodents have little contact with presumptive offspring, at least until young
emerge from the nest, and contact with young might be actively discouraged. Female meadow
voles prevented males from interacting with pups in a semi-natural runway system (McGuire
and Novak, 1984).
Paternity may be relatively certain in some species, but less so in others in the same genus
(Birdsall and Nash, 1973; Foltz, 198la, 1981b). Behavior of males toward young should be
influenced by the degree of uncertainty. Available data are ambiguous as to the ability of males
that have not cohabited in the nest to recognize young they have sired. Males that do not share
a nest with females and their litters might recognize offspring directly (e.g., through matching
of chemical phenotypes), through association with the maternal female, or through the appear-
ance of young as weanlings within the paternal home range. Encounters with their offspring are
probable in sedentary males, but recognition is less likely where males shift ranges after breeding.
Males appear unable to distinguish their offspring from those of others in some ground squirrels
(Michener, 1980; Sherman, 1977, 1980).
The strongest evidence for paternal recognition might be the fact that although males of many
species cannibalize young, males have rarely been observed to kill young that they sired. Males
could benefit from infanticide if they killed and cannibalized young for their nutritional value,
or as a means of assuring or accelerating paternity (Elwood, 1983). Labov (1980) found no
difference in the proportion of pups killed by same-strain and other-strain males when female
house mice were placed in the males’ cages 3 days prepartum, but his design did not distinguish
between stud and non-stud males. Rates of infanticide were low in all cases. Stud male Dicros-
tonyx introduced into laboratory cages containing the maternal females and their own young
did not attack the young, whereas non-stud males acted infanticidally in the same situation
(Mallory and Brooks, 1978; Webster et al., 1981). It is not clear whether infanticide in such cases
involves the paternity of the young in question, or is simply induced by the maternal attack on
the non-stud male under conditions of confinement in small spaces, although it has been observed
in moderate-sized outdoor pens (Heske and Nelson, 1984). Immigrant male Spermophilus parryii
tend to kill young in the process of establishing themselves (McLean, 1983). As females are
monestrous there is no immediate mating advantage to this behavior. If female young (potential
mates) are killed along with males, infanticide could reduce rather than increase the fitness of
immigrating males. McLean reported that male S. parryii defended territories primarily during
the period when young were most vulnerable to infanticide, and that removal of presumptive
sires increased the probability of infanticide. Sires appeared to act as lookouts during the period
of lactation (McLean, 1983).
When males cannot recognize their own offspring, the best course might be to tolerate all
Testing RFH 69
prepubertal young. Tolerance for prepubertal offspring has been evident in observations of male
behavior in Peromyscus (Eisenberg, 1962; Horner, 1947; Howard, 1949), Onychomys (Horner
and Taylor, 1968), and Microtus (Thomas and Birney, 1979). In the laboratory, males have been
observed to hover over, lick, and retrieve offspring in Peromyscus (Horner, 1947; McCarty and
Southwick, 1977a), Onychomys (Horner and Taylor, 1968; McCarty and Southwick, 1977a,
1977b), and Rattus (Horner and Taylor, 1969). Adult male meadow voles investigated young
introduced into their home cages, but were not aggressive toward them; this was in contrast to
lactating females, which were aggressive toward unfamiliar young (Boonstra, 1984). McGuire
and Novak (1984) reported similar tolerance of weaned young by male meadow voles within a
semi-natural runway system. Paternal tolerance of offspring is variable among Microtus species
(McGuire and Novak, 1984, 1986; Oliveras and Novak, 1986; Thomas and Birney, 1979; Wilson,
1982). In the absence of dedicated studies in the field, it appears that in nature the behavior of
resident males toward sexually immature young also tends toward neutrality. This is not surprising
because males in most species appear to have little contact with young.
Other than guarding against infanticide, it could be that the greatest contribution a paternal
male can make to the welfare of offspring of either sex is to facilitate the inheritance of the
paternal home range. As in those birds where offspring are retained as helpers (Brown and Brown,
1984), retention of young in the paternal territory could increase survival and future reproduction.
Paternal behavior toward offspring can be expected to change when maturing offspring become
potential mates or potential competitors for matings, and when paternal reproductive potential
is exhausted. In general, offspring should be treated as relatives capable of making a contribution
to paternal fitness.
There is no evidence of barriers to inbreeding in the behavior of paternal males toward female
offspring. Insofar as paternal pheromones accelerate puberty of daughters (Bronson, 1979), the
available evidence on behavior and function of males with respect to daughters suggests that
inbreeding is likely to be facilitated.
Svare (1981) commented that male aggression as a paternalistic behavior had been so little
studied that discussion of the topic was precluded. There are a few indications of active nepotism
by male rodents, but it is not clear that investigators have looked for it. I have found no studies
that deal specifically with paternal behavior as an active contribution to philopatry. Early
hibernation of breeding males in some ground squirrels might relate to competition among males
(Michener, 1984), but could secondarily benefit offspring by reducing competition in the critical
period before their first hibernation. Declining male aggressiveness in polyestrous species might
be associated with recruitment of young that will overwinter, but the relevant male patterns
might be explicable on other grounds, and benefits for offspring, or their fathers, have not been
quantified. “Neutrality” sums up the bulk of what is known about male-offspring relationships
in nature.
Competition and Aggression in Female Rodents
Female aggressiveness, like that of males, is associated with reproductive activity, but has
received much less attention from ecologists and ethologists. This probably is because females
are less easily induced to fight in arenas. The aggressiveness of adult females normally declines
outside the breeding season, but persists when breeding is extended. For example, Ylonen and
Viitala (1985) reported that female Clethrionomys remained aggressive when breeding continued
over winter.
Although Hyde and Sawyer (1977) reported a peak in female aggressiveness during proestrus,
it is evident that resident females are not required to compete for copulations. Pregnancy rates
among adult female rodents tend toward 100% (e.g., Dobson, 1982; Mihok, 1981) and female-
biased sex ratios in ground squirrels do not result in lower pregnancy rates (Michener and
Michener, 1977). Removal of sexually active males did not affect density or reproductive status
of female Microtus pennsylvanicus, and exclusion of adult female immigration by resident
females was not dependent on the density of breeding males (Boonstra and Rodd, 1983).
70 Rodent Dispersal
Female aggressiveness varies with gestation and lactation in ways that reflect both resource
requirements and defense of current investment in offspring. Aggressiveness increases with
progesterone level (Gleason et al., 1979), and is highest during pregnancy and lactation (Boonstra,
1984; Burt, 1940; Festa-Bianchet and Boag, 1982; Gleason et al., 1980; Nicholson, 1941). Female
ground squirrels apparently do not establish territories until pregnant (Holmes and Sherman,
1982). It is during gestation and lactation that nutritional requirements of females are greatest
(Sadleir et al., 1973); lactation is also the time when investment in vulnerable nest young is high.
Heightened aggressiveness in females with nest young has been reported by Fleming (1979),
Gray (1979), and Mallory and Brooks (1980). Female Mus in the laboratory are most aggressive
toward unfamiliar juveniles during the first 2 weeks postpartum (Gray, 1979). Non-lactating
female Microtus pennsylvanicus ignored unfamiliar young introduced into their home cages
but lactating females were aggressive toward them (Boonstra, 1984). Female Peromyscus leu-
copus in their home cages showed the greatest aggressiveness toward diestrous conspecific females
when in late pregnancy and during the middle portion of lactation. When encounters took place
in a neutral cage there was no difference in aggression over the course of pregnancy, and increased
aggression was evident only on day 5 postpartum (Gleason et al., 1980). This result illustrates
the importance of location, and re-emphasizes the point that “neutral arenas’ can give misleading
results.
Ostermeyer (1983) has provided a detailed review of the literature on female aggression as it
is specifically related to pregnancy and lactation. Such aggression has been recorded in 14 rodent
genera. It is viewed as a special category (“maternal aggression”) and characterized by a brief
latency to attack, high intensity, and damaging attack to vulnerable areas. Maternal aggression
has one peak in the first third of pregnancy, and a more intense peak late in the first third or
early in the middle third of the lactation period.
Increased aggressiveness during lactation might serve both to conserve resources and to protect
reproductive investment from intruding conspecifics. In the laboratory, maternal aggression is
most often directed against unfamiliar males, and is site (home cage) dependent but not dependent
on the presence of pups. Because females encountering unfamiliar males under laboratory
conditions in the first few days of pregnancy could abort their litters, and because pups might
be killed and eaten under these conditions by males that did not sire them, the implication is
that the primary function of maternal aggression is protection of maternal investment. Ostermeyer
(1983) tends to accept this conclusion. However, field data are largely lacking and it is possible
that both pregnancy block and male infanticide are results of the agonistic interactions generated
by the laboratory situation, rather than the evolutionary precursors of maternal aggressiveness.
Mallory and Brooks (1980) have suggested that infanticide by intruding females might be the
main threat toward which aggression of lactating females is directed.
There is a strong case for a relationship between female aggression and the acquisition and
retention of resources. Female home ranges are more commonly exclusive of same-sex breeding
residents than are those of males (Blair, 1951; Bondrup-Nielsen and Karlsson, 1985; Brooks and
Banks, 1973; Bujalska, 1973; Daly and Daly, 1975; Dixon, 1958; Eisenberg, 1975; FitzGerald
and Madison, 1983; Howell, 1954; Jannett, 1980, 1981b; Kawata, 1985b; Madison, 1980a, 1980b;
Metzgar, 1979; Mihok, 1981; Perrin, 1981; Reich and Tamarin, 1980, 1984; Sherman, 1980;
Smith, 1978; Stoddart, 1970; Tanaka, 1953). Overlapping ranges of breeding females are reported
relatively rarely (Behrends et al., 1986; Morris, 1955; Myllymaki, 1975; Ostfeld, 1986; Wolff,
1980). When they do overlap, the relative extent of overlap might be less than that in males
(Behrends et al., 1986). Analyzing sequential catches of Microtus pennsylvanicus in multiple-
capture traps, Reich and Tamarin (1984) found that breeding females were the population
component most likely to occur singly. In a study of sequential captures in traps scented by a
previous occupant, breeding females were rarely caught in traps in which a different breeding
female had been caught previously. Multiple captures of female M. pennsylvanicus have been
observed less frequently than would be predicted from the frequency of females in populations
(Getz, 1972; Slade, 1976).
Testing RFH 71
There is ample evidence that nutritional resources are important to females. Pfeifer (1982a)
reported that female Spermophilus holding territories on which earlier snow melt had led to
earlier vegetative growth produced the most young. Individual reproductive success of female
marmots is significantly associated with food availability (Andersen et al., 1976) and decreases
with harem size (Armitage, 1986b; Downhower and Armitage, 1981). In many hibernating
sciurids, female emergence is timed to coincide with the spring flush of vegetative growth
(Michener, 1984). Where the growing season is very short, emergence and parturition of female
yellow-bellied marmots can occur earlier, allowing young to obtain sufficient nutrition to fuel
winter metabolism.
Experimental supplementation of food supplies usually caused increased population density
and/or induced immigration (Cole and Batzli, 1979; Flowerdew, 1972; Gilbert and Krebs, 1981;
Hansson, 1971; Mares et al., 1976; Sullivan et al., 1983; Wolff, 1986). Young and Stout (1986)
reviewed 13 food-supplement studies in Peromyscus and reported that supplemental food in-
creased the minimum number known alive (MNA) on study grids in most, but not all, studies.
Their own data showed that supplemental food increased the MNA primarily through an increase
in transient P. gossypinus, but did not increase persistence of juveniles, and apparently did not
affect the density of Ochrotomys. Wolff (1985a) reported that food supplements caused a re-
duction in the size of home ranges of P. leucopus and P. maniculatus until an apparent minimum
size was reached, after which range overlap and aggressive interactions were evident. Taitt (1981)
reported that food supplements maintained reproduction in populations of Peromyscus despite
winter weather.
Gurnell (1983) viewed most experimental attempts to alter the demography of tree squirrel
populations through supplemental feeding as inconclusive. Krebs and DeLong (1965), Cole and
Batzli (1978), and Desy and Thompson (1983) all failed to halt population declines in Microtus
by supplying supplementary food. In other studies, food supplements have facilitated repro-
duction (Andrzejewski, 1975; Bendell, 1959; Cole and Batzli, 1978; DeLong, 1967; Flowerdew,
1972; Sullivan et al., 1983; Taitt, 1981; Taitt and Krebs, 1981, 1983; Watts, 1970) and increased
the proportion of resident females breeding (Desy and Thompson, 19838; Ford and Pitelka, 1984;
Taitt et al., 1981). Reproduction-enhancing effects of food supplements do not require an increase
in the density of breeding males (Fordham, 1971). Radiotelemetry revealed that home ranges
of female M. californicus decreased in size when food was supplied, that overlap of ranges
increased, and that some females shifted ranges into the area where supplemental food was
available (Ostfeld, 1986). In northern Finland, female M. oeconomus shifted nest sites to follow
the progressive appearance of new vegetation behind receding spring meltwaters (Tast, 1966).
Seasonal appearance of new vegetation may control vole reproduction directly in at least some
species. Seasonal activation of female M. montanus can be induced through physiological re-
sponses to intake of substances associated with seed germination and growth of vegetation (Berger
et al., 1981; Negus and Pinter, 1965; Negus et al., 1977).
There is room for a great deal of further study of the role of nutrition in the strategies of
female microtines (Batzli, 1985). Survival of female Microtus can vary with patch quality, and
increased quality through supplementary food, watering, or fertilizing generally has resulted in
an increase in density, litter size, and persistence of adult females (Ostfeld, 1985a). Myllymaki
(1977b) concluded that female Microtus agrestis were capable of coming into breeding condition
whenever high quality food was abundant. In a season of high density and food abundance,
female Dipodomys spectabilis tended to abandon natal sites to offspring, thereby increasing
offspring survival without apparent cost to themselves (Jones, 1986).
The RFH predicts that female aggressiveness in defense of resources would be high in times
when resource demands would increase or peak, and that resource defense should be directed
toward other females because they represent greater threats to resource availability than do
males. Pre-eminence of nutritional resources should place a premium on habitat selection by
females.
The limited comparisons of habitat selection in males and females to date have been incon-
WZ Rodent Dispersal
sistent. Bowers and Smith (1979) evaluated habitat quality on the basis of water potential in the
vegetation in arid areas of western North America and concluded that female Peromyscus chose
habitat of higher quality than did males. Morris (1984), working in more mesic habitats in the
northeast, concluded that males selected the higher quality habitats. Krohne et al. (1984) noted
a significant female-biased sex ratio among P. leucopus settling in a seasonally available habitat,
and a male-biased sex ratio among individuals moving between trapping grids inhabited through-
out the year. This is unexpected under the RFH, but might reflect a focus on mates as resources
by male transients, and a focus on uncontested access to food and other “habitat” qualities by
female transients.
Female aggressiveness can be reduced under appropriate circumstances. McShea and Madison
(1984) observed sharing of nests by two lactating Microtus pennsylvanicus in spring and suggested
that thermal advantages at this time (when resources were perhaps superabundant) might make
sharing an advantageous strategy for closely related females. Cooperative nesting was not observed
later in the season, when resources might have been in less abundant supply. Overlapping female
ranges are found primarily in the more social of the sciurids (Armitage, 1975; Hoogland, 1982;
King, 1955). The data from this group suggest that whenever such overlap of female home ranges
is observed, the maturity and genetic relationship of the females involved should be taken into
account. McLean (1982) found that among arctic ground squirrels close female kin (sisters,
mothers, and daughters) had more overlap of home ranges and interacted more amicably than
unrelated individuals. Close female kin also clumped their young on emergence. Distant relatives
that had not associated on emergence were intermediate in these characteristics between close
kin and unrelated individuals.
Food resources may not be the only focus of female competition. Pfeifer (1982a) found that
female reproductive success in ground squirrels varied with the quality of the maternity burrows.
Poor burrows might increase the chance of infanticide by neighboring females, who could increase
their own fitness by killing the litters of unrelated neighbors (Sherman, 1981, 1982). Sherman
(1981) suggested that infanticide by female Belding’s ground squirrels that had lost their own
litters to predation could represent a competitive move by means of which the perpetrator
replaces an unrelated female on a safer burrow site.
Michener (1980) reported that differential female reproductive success in Spermophilus rich-
ardsonii was achieved by production of female-biased litters. She considered that, in such female-
philopatric and matrilineal species, investment in daughters and nepotism toward them is highly
advantageous. The utility of this strategy may be limited by effects of resource shortage on
survival of offspring (Downhower and Armitage, 1981). However, reproductive success of sons
has not been examined in sufficient detail to permit comparison.
Female aggression, like that of males, is associated with the breeding season. Unlike that of
males it has a cyclic expression associated with gestation and lactation. This is specifically referred
to as maternal aggression, and is closely related to investment in young. Females compete for
resources, and female territoriality can be expected to function in defense of both resources and
young. These observations suggest that female aggression could significantly affect both emi-
gration and immigration.
Resident Female Nepotism
Although male rodents often have little opportunity to contact young, females can readily
identify and form bonds with their young at birth and are generally able to recognize their own
offspring (Beach and Jaynes, 1956a, 1956b; Downhower and Armitage, 1981; Holmes and Sher-
man, 1982; Michener, 1973; Michener and Sheppard, 1972; Sherman, 1977, 1980). Mother-young
associations established at birth and during lactation often continue after weaning. The certainty
of relationship, the prolonged period of association, and the high maternal investment all underlie
maternal nepotism. Options open to the mother include conservation of young at the natal site,
selective export of offspring, inbreeding, avoidance of inbreeding, or manipulation of offspring
Testing RFH WS
in ways that optimize between inbreeding and outbreeding (Moore and Ali, 1984). Mother-
young recognition makes possible the formation of persistent matrilineal groupings of related
individuals in which there can be exchange of altruistic behaviors.
Kin recognition and maternal nepotism have been studied in greatest depth among ground
squirrels (Davis, 1984; Sherman, 1980; Sherman and Holmes, 1985). Recruitment, where carefully
documented, appears to consist largely of individuals born into local groupings, whether in
ground squirrels (Hoogland, 1981; Michener, 1983b; Sherman, 1977, 1980) or house mice (Li-
dicker, 1976).
Females initially behave nepotistically toward their entire litters, regardless of the sex of the
offspring. Nevertheless, as predicted by the RFH, recruitment from a given litter is usually sex-
biased. Associations between mothers and daughters are more persistent than those between
mothers and sons, reducing the likelihood of mother-son matings, favoring the formation of
mother-daughter clusters and matrilines, and increasing opportunity for father-daughter matings.
Mother-daughter relationships can be readily observed in some ground squirrels. In such cases
females persist in cohesive behavior toward their daughters even as they grow older (Armitage
and Johns, 1982). In species that hibernate, mutual recognition and bonding between mothers
and daughters remain evident after emergence (Michener, 1974; Michener and Sheppard, 1972).
Adult female Columbian ground squirrels allowed daughters to inherit parts of their breeding
territories, and if a resident female shifted her range it was usually taken over by a daughter
(Harris and Murie, 1984). Because mothers were dominant to yearling daughters, maternal moves
were not forced by filial competition; maternal range shifts appear to be a form of parental
investment.
Matrilineal groupings in Speromophilus columbianus typically included an adult female, a
3-year-old female, and a 2-year-old female. More than 75% of 2- to 4-year-old females had at
least one adult female relative in the same breeding group (King and Murie, 1985). Female
ground squirrels will attack unrelated young but are less inclined to attack those of their own
daughters (Sherman, 1977). Female black-tailed prairie dogs are much more likely to behave
amicably toward members of their own coteries than toward members of neighboring coteries
(Hoogland, 1981).
Although females behave so as to favor recruitment of daughters, maternal behavior appears
neutral or negative with respect to recruitment of sons. Most resident female yellow-bellied
marmots are recruited from their natal colonies, but most of the breeding males are recruited
from other colonies (Armitage, 1984; Schwartz and Armitage, 1980). Yellow-bellied marmot
colonies thus persist as matrilines for many years (Armitage, 1986b). The result of maternal
nepotism in all intensively studied ground squirrels is that the fundamental social unit is the
“mother-headed family” (Michener, 1983b). Work on South American caviomorphs occupying
similar niches (Rood, 1970) suggests that this generalization applies to that group as well.
Relatively little effort has so far been devoted to determination of the extent of nepotism in
other rodents. Evidence of female nepotism toward daughters, similar to that observed in ground
squirrels, has been inferred for microtines (Frank, 1957; Jannett, 1978; Madison, 1980b; Madison
et al., 1984; Wolff, 1980). The primary cause of bias in recruitment in these rodents seems to
be male emigration (e.g., Myllymaki, 1977a, 1977b). Young Microtus of both sexes are much
more likely to be caught in multiple-catch traps with adult females than with adult males (Slade,
1976).
Abdication of the maternal home range as a form of maternal nepotism has been suggested.
Resident females sometimes shift their own homesites, leaving parts of their ranges to their newly
weaned litters in Dicrostonyx (Brooks and Banks, 1973), Microtus (Jannett, 1978, 1980; Madison,
1980b; McGuire and Novak, 1986; Myllymaki, 1977a), Tamiasciurus (Price et al., 1986), Pero-
myscus (Howard, 1949), and Dipodomys (Jones, 1986). Jones (1986) reported that survival of
philopatric young was higher when maternal Dipodomys spectabilis abandoned the natal mound
and shifted to another mound on the margin of the natal range compared to that when the
74 Rodent Dispersal
female simply disappeared. Nepotism in female D. spectabilis appeared to be impartial with
respect to sex. Jones found no difference in the proportion of male and female offspring acquiring
natal mounds. The cost to maternal females appeared to be slight. Females moved less than the
mean width of a territory, and the survival of those that moved was as high as that of those that
did not. Maternal abdication in this species would not reduce the probability of mother-son
matings.
Madison et al. (1984) observed that at the end of the breeding season Microtus pennsylvanicus
in outdoor enclosures formed matrilineal groups in which there was selective retention of males.
Communal winter nests were observed to develop around a female and included her immature
young and males from the surrounding area. Relatedness was not determined in communal nests
shared by lactating M. pennsylvanicus in spring (McShea and Madison, 1984) so the persistence
of matrilineal groupings beyond the non-breeding season is uncertain.
Behaviorally, maternal nepotism is modified in response to density. Maternal females might
become more aggressive toward their offspring as density increases, or they might cease to
abdicate nest sites to their litters (Hoogland, 1986; Jannett, 1978).
Given the general evidence of maternal nepotism toward daughters in the wild, what signif-
icance is to be attached to the observation that close confinement with a maternal female will
inhibit sexual maturation of female young in the laboratory? Getz et al. (1983) suggested that
female pheromones blocking sexual activation of female young would serve to restrict breeding
to a single pair in a social group. Maximization of direct fitness at the expense of reproductive
contributions from offspring is understandable if the retained young can contribute in some way
to parental reproductive success. This analysis could apply also to M. pinetorum, because in
most cases only a single female in a colony is reproductive (FitzGerald and Madison, 1983). The
extreme of such pheromonal inhibition is reached in Heterocephalus glaber, in which many
females are non-reproductive throughout their lives, carrying out specialized tasks in a colony
in which a single large female produces all young (Jarvis, 1981). Waser and Jones (1983) have
pointed out that H. glaber may represent the end of a continuum in social evolution within the
Bathyergidae.
Although it would not be surprising to find that in most species maturation of young females
can be inhibited by exposure to maternal pheromones under laboratory conditions, it is unclear
how common the phenomenon is in the wild. Exposure to the urine of maternal or other adult
females blocks the activation of virgin female Microtus ochrogaster by males (Carter and Getz,
1985; Getz et al., 1983). Getz (1978) proposed that suppression of maturation in female young
was a means of maintaining low densities in stable habitat. Superficially, at least, this is a pattern
that would increase the persistence of a group at the expense of individual success.
Interpreted on the basis of maternal fitness, instances of suppression by maternal pheromones
can be viewed as a means of conserving offspring and of furthering nepotism. In circumstances
where maternal females retain considerable residual reproductive value, maturation of female
offspring portends competition, but expulsion of offspring is costly in terms of offspring survival.
The RFH encourages a postulate that selection would favor inhibition of juvenile development
as a means of regulating export of offspring so as to maximize the chances that they will survive
to contribute to the future gene pool at a later date. Observations on a small island (Bujalska,
1970, 1971, 1973) suggest that inhibition of daughters in response to density or resource shortage
might have this effect, because disappearance of a breeding female leads to reproduction by a
previously inhibited young female. On the other hand, Snyder (1962) reported that removal of
adult females from a free-living woodchuck population delayed, rather than accelerated, the
maturity of juvenile females.
Maternal nepotism is at least widespread, if not universal, among rodents. It conforms to the
predictions of the RFH and can be interpreted as an example of parental manipulation of the
philopatry-emigration option for offspring. If females are generally nepotistic, and preference
is directed toward daughters, dispersal becomes a matter of emigration from, and immigration
into, matrilineal groups. The observation that female nepotism is directed primarily toward
Testing RFH 75
daughters also provides a rationale for the observation that female grouping establishes the basis
for polygyny (Wittenberger, 1980).
Inhibition of Immigration by Residents
Evidence of inhibition of immigration falls into three categories: appearance of new individuals
when residents are removed; location-dependent dominance by residents; and avoidance of
residents by non-established individuals. To a varying degree the information in these three areas
can be detailed with respect to factors that modify the probability that immigration will be
successful.
Removal studies provide circumstantial evidence that the presence of residents prevents set-
tlement and immigration of transients. New settlers (potential immigrants) typically appear
immediately in trap samples when residents are removed from field populations. Removal studies
have resulted in increased capture of unmarked individuals in the genera Apodemus (Flowerdew,
1978), Peromyscus (Fairbairn, 1978a; Healey, 1967; Sadleir, 1965), Clethrionomys (Watts, 1970),
Microtus (Baird and Birney, 1982a, 1982b; Beacham, 1980b; Boonstra, 1978; Hilborn, 1975;
Myers and Krebs, 1971), Sigmodon (Joule and Cameron, 1975), and Reithrodontomys (Joule
and Cameron, 1975).
Although it is clear that removal of trappable individuals leads to the appearance, in traps,
of previously unencountered individuals, the origin of the new individuals is not specified. We
cannot be sure that the presumed immigrants were drawn from a pool of individuals that
originated elsewhere. Studies that made concurrent use of conventional live traps and pitfall
traps (e.g., Beacham, 1979b; Beacham and Krebs, 1980; Boonstra and Krebs, 1978; Boonstra and
Rodd, 1984) have shown that conventional removal studies fail to distinguish among neighbors
making sorties outside their home ranges, individuals present but inhibited from entering traps,
and transients. Simple removal studies show only that the presence of trap-prone individuals
inhibits capture of a broad spectrum of other individuals.
The question of whether residents prevent establishment of transient individuals can be an-
swered by means of introduction experiments. Introduced animals rarely settle in undisturbed
populations, but are more likely to settle if residents are removed. Smyth (1968) compared
persistence of marked Clethrionomys released in a control area and in an area from which adult
males and non-lactating adult females had been removed. During the breeding season, persistence
of adults released on the removal area was higher than on the control. Persistence of young was
less affected by removal of adults. Marked young males survived poorly on both areas, but
introduced voles in other categories persisted longer on the removal area. Flowerdew (1978) also
combined removal and introduction and compared the persistence of experimentally introduced
wood mice (Apodemus) in areas where residents were present, and in areas where residents had
been removed. Again, establishment of these potential immigrants was more likely in the areas
where residents had been removed.
The interaction of residents and presumed or known non-residents has been observed most
often in laboratory situations. Conventional arena tests between known residents and presumed
non-residents (e.g., Reich et al., 1982) suffer from the basic flaw that neither of the test individuals
is resident in the “neutral” arena. Despite this, residents are most often dominant. In a major
improvement in arena testing, Wolff et al. (1983) staged encounters in the field between resident
and non-resident Peromyscus.
In confrontations observed by Barash (1981), resident male Marmota calligata were successful
in repulsing intruders. In another study (Yahner, 1978), resident Tamias striatus of both sexes
successfully excluded other conspecifics from core areas around their burrows.
Hill (1966) observed the response of house mice residing in granaries to caged and unrestrained
introductions of individuals moved from neighboring populations. Resident mice attempted to
enter the cages as if to attack the introduced mice. When Hill released unrestrained strangers
they often left the granary even before encountering residents. The majority of those that were
not seen to leave of their own volition were attacked by residents (both sexes) and driven out.
76 Rodent Dispersal
None of the 10 males and 10 females released in these observational studies became resident.
Hill’s approach demonstrated that residents actively and effectively resist the establishment of
strangers.
Encounters with residents might not be required to prevent transients from settling. Despite
the multitude of studies reporting fighting in arenas, it is not yet clear that fighting (as opposed
to avoidance or chasing) is commonly involved in exclusion of potential male immigrants. Where
egress is an option, non-residents might retreat rather than engage in combat. It has been observed
in both field and laboratory that transient or subordinate individuals respond to resident or
dominant conspecifics by avoidance (e.g., Armitage, 1974; Parmigiani et al., 1981). If arena size
is increased, for example, unfamiliar male Peromyscus leucopus avoid encounters (Vestal and
Hellack, 1977). Ostfeld (1985b) also observed that although unfamiliar male Microtus californicus
exhibited more aggression in small arenas than did females, reproductive males were more likely
to flee non-aggressive approaches of same-sex adults than were females when the interaction
occurred in a larger area. Price et al. (1986) noted that female Tamiasciurus that had lost their
territories became wanderers until such time as they were able to discover a vacant territory.
Occupancy of the vacant territory was promptly signaled by frequent calling.
If avoidance is the rule in nature, scent marks or visible or audible displays by residents could
be adequate to cause potential immigrants to move on, avoiding actual confrontations. Although
male scent marks do not appear to function as sex attractants, the quality and quantity of scents
produced by male rodents generally peak during the breeding season (Stoddart, 1978). Urine is
the predominant substance used by males in scent marking. Male urine marking has important
functions in cueing female reproductive activity in the house mouse (reviewed by Bronson, 1979),
but it also has adverse effects on subordinate males (Jones and Nowell, 1974), lending support
to the hypothesis that male scent marking could also have an important role in excluding potential
competitors from scent-marked home ranges.
Introduced females are more likely to become established in introduction experiments than
are introduced males (e.g., Anderson, 1965; Redfield et al., 1978b). This suggests that resistance
of residents may be specific to the sex of both residents and potential immigrants. Michener and
Michener (1977) recorded male immigration in a Spermophilus population with a low proportion
(0.3/1) of breeding males. Resident female marmots are apparently able to repel intruding
females, but are dominated by intruding males. Males repel intruding males, but accept intruding
females (Armitage, 1975). In Microtus pinetorum, immigration occurred only when no adult
resident of the immigrant’s sex was present in the colony (FitzGerald and Madison, 1983). Boonstra
and Rodd (1983) found that removal of breeding adult Microtus stimulated immigration by the
same sex, but not by the opposite sex. Redfield et al. (1978a, 1978b) argued that because potential
immigration was far in excess of actual recruitment, residents must inhibit immigration. They
concluded, however, that removal of female M. oregoni and M. townsendii did not stimulate
female immigration, and that male removal did not stimulate male immigration. Their results
might have been affected by the fact that sex ratios of the two species were being manipulated
simultaneously.
Restriction of immigration has often been attributed largely or exclusively to the aggressiveness
of males (e.g., Adler et al., 1984). Sadleir (1965), Healey (1967), and Flowerdew (1978) all
reported that removal of resident males facilitated the immigration of conspecific Peromyscus.
Flowerdew (1974) obtained parallel results in experimental removal of male Apodemus. If males
compete for copulations, male residents would be expected to be effective in excluding male
immigrants, but to be less effective or ineffective in excluding female immigrants. This prediction
is supported by the fact that unfamiliar males of most species of rodents will fight if placed in
small cages without cover or possibility of egress, whereas males are less likely to attack unfamiliar
females under these “arena” conditions (e.g., Gipps, 1984).
The pattern of same-sex exclusion might not be consistent across species. Cranford and Derting
(1983) stated that in a 6l-cm? arena, male Microtus pinetorum were more aggressive than
females in within-sex encounters, but that female M. pennsylvanicus were more aggressive than
Testing RFH 77
males under the same circumstances. Sexual distinctions probably arise only with the maturity
of the young. Halpin (1981) observed no significant difference among responses of adult male
Peromyscus to male and female juveniles except that males showed more cohesive behaviors
toward older juvenile females than toward younger ones.
There are a few exceptions to the results suggesting that male residents inhibit primarily or
exclusively the immigration of adult males. For example, Gavish et al. (1983) found that sexually
experienced male M. ochrogaster were aggressive toward unfamiliar virgin females in dyadic
encounters in the laboratory.
In species in which females are monestrous, males might have relatively minor effects on
immigration. Dobson (1979) was not able to induce an influx of immigrants by removal of
resident male Spermophilus beecheyji. In other species of Spermophilus, males leave their breeding
ranges when mating is over (Holmes and Sherman, 1982; Michener and Michener, 1977). Male
S. parryii, however, continue to defend territories during the period when females are pregnant.
There is need for further study on the role of males in excluding immigrants. The available
information implies that the role of male aggression in inhibiting immigration can be expected
to vary with the sex, age, and reproductive status of the potential immigrant, as well as seasonally
and with the mating system and other natural history parameters of the species. In this context,
as in the case of male competition for copulations, the nature of territorial behavior needs further
definition and exploration. The valid generalizations with respect to the role of males in inhibiting
immigration appear to be that male aggressiveness is likely to: 1) be effective primarily in
excluding sexually mature males during the breeding season; 2) have little impact on immigration
of adult females and sexually immature young of either sex during the breeding season; and 3)
have little or no effect on immigration of any category of conspecifics outside of the breeding
season. Exceptions can occur where males guard hoarded food, lactating females, or nest and
weanling young. Getz and Carter (1980) suggested that transient male M. ochrogaster can be
driven off by resident males before there is an opportunity for virgin females (daughters of the
residents) to be sexually activated. Such behavior would restrict outbreeding and conserve the
potential for incestuous matings.
In several studies, aggressive tendencies of females could be specifically related to inhibition
of immigration. Female yellow-bellied marmots repel intruding females from their colonies
(Armitage, 1986b). Female Microtus have been found to be tolerant only toward their own
offspring and toward familiar resident males. Comparing immigration of M. townsendii into
plots from which residents had not been removed with movement into male-removal and total-
removal plots, Boonstra (1978) concluded that the higher rate of appearance of immigrants in
the total-removal plots was due to the absence of female residents. Boonstra and Rodd (1983)
showed that the presence of breeding females restricted recruitment of other breeding females,
and removal of resident females induced settlement of sexually mature females during the latter
part of the breeding season. Restriction of female recruitment by breeding females was not
dependent on the presence of males. Rodd and Boonstra (1984) found that reduction in density
of overwintering M. pennsylvanicus induced an increase in female home range size during the
subsequent spring breeding period. Gipps et al. (1985), however, were unable to detect any
difference in the immigration rate on control and experimental grids following removal of resident
female Clethrionomys glareolus at the start of the breeding season.
Metzgar (1971) found that opportunity for female Peromyscus leucopus to settle was negatively
correlated with the density of resident females and that transient females could settle only when
vacancies were created by disappearance of female residents. Female P. leucopus were more
aggressive toward intruding females than resident males were toward unfamiliar males.
Exclusion of immigrants is probably strongly dependent on the reproductive state of residents.
Male aggressiveness usually declines following the breeding season. Behavior of resident males
then could have little or no effect on male immigration. Boonstra and Rodd (1983) found that
it was primarily at the start of the breeding season that removal of breeding male Microtus led
to immigration of older adult males on their open grid. Later in the season removal of resident
78 Rodent Dispersal
males resulted in immigration of sexually mature male young of the year. By removal of females,
Boonstra and Rodd also showed that the effectiveness of breeding males in inhibiting recruitment
at any time was dependent on the presence of breeding females. This implies that in polyestrous
species in which pregnancy and birth of young extend beyond the decline in male aggressiveness,
recruitment of the last litter and immigration of young of either sex may be unaffected by
aggressive behavior of resident males. Immigration into matrilineal clusters of Microtus has been
observed to occur only after the breeding season (Madison et al., 1984; Wolff and Lidicker, 1981).
Exclusion of immigrants by a resident parent should reduce the probability that the range and
its resources will become available to a non-relative. If this behavior thereby increases the
probability that the parental range will be inherited by an offspring it is a form of altruistic
behavior. As Smith and Ivins (1983) pointed out, it constitutes an indirect form of parental care.
Avoidance of contact and other expressions of male incompatibility appear to inhibit male
immigration in Peromyscus maniculatus prior to the onset of breeding and throughout the period
when matings are available (Healey, 1967; Sadleir, 1965), but Metzgar (1971) concluded that
this was not the case in P. leucopus. He felt this might be because the large home ranges occupied
by males prevented effective exclusion of other males. Range size is more likely to prevent
exclusion of transients than of immigrants, however, since settlers can be detected and confronted
even where the range is large.
Eibl-Eibesfeldt (1950) observed that house mice were able to establish themselves in a building
only if they were able to find a defensible corner and persist there through an initial period of
resident hostility. His observation implies that immigration can be influenced by the complexity
of the habitat. Defensible space might be more easily located in nature than in simpler envi-
ronments.
Female house mice introduced into occupied fields by Myers (1974) failed to establish residence,
but those introduced into occupied chicken coops by Baker (1981) did so. The success of Baker
in introducing house mice into chicken coop populations where the rate of turnover was high
was not matched in low-turnover granary populations (Anderson, 1965; Hill, 1966).
Is resistance to immigration density-dependent? Wolff (1985a) reported that the aggressiveness
of resident Peromyscus toward non-residents varied with density. At high density the residents
were aggressive and dominant. At low density, however, aggressive behavior was rare. This result
is significant because it suggests that resistance to immigration might become more intense as
density increases and might decline as density decreases. Hestbeck (1986) found that the effec-
tiveness of resident voles in inhibiting movement through an area increased with density. Carter
and Getz (1985) reported, however, that pairs of Microtus ochrogaster excluded strangers more
effectively at low densities than at high densities.
Resident bannertail kangaroo rats (Dipodomys spectabilis) are solitary, occupying individual
mounds which they defend by footdrumming. Juveniles either take over vacated mounds or
establish new mounds in the interstices between those that are occupied. As distances between
occupied mounds decrease, residents visit neighboring mounds less and drum more often, sug-
gesting that possession of a territory is more actively advertised as density increases (Randall,
1984).
Taitt and Krebs (1982) were surprised to observe increased female immigration when they
treated female Microtus townsendii with testosterone implants. This apparently anomalous result
is understandable if viewed in the context of the overall masculinization induced by the male
hormone. If implants caused the treated females to behave as males, the quantum of “female”
behavior in the area was thereby reduced and the observed immigration could have been
predicted on the basis of the RFH argument that density is largely under female control.
The references cited above indicate that the presence of residents inhibits other conspecifics
from becoming resident, and that the inhibition might be mediated through aggressive behavior
or display or both. Despite the flaws in the most commonly used removal and arena techniques,
it seems safe to conclude that residents inhibit immigration of same-sex adults. The situation is
less clear with respect to juveniles and subadults. Resistance to immigration is likely to be seasonal
in seasonally breeding species. It might be influenced by the availability of defensible space for
Testing RFH 79
immigrants, and by the influence of density on the behavior of residents. Field experiments,
possibly based on the approaches of Smyth (1968), Flowerdew (1978), Hill (1966), and Wolff et
al. (1983), which explore the role of relatedness and season in the resistance offered by residents,
will be helpful. Removal of single individuals or small groups (Price et al., 1986) also could be
more informative than the mass removal technique that has been used in the past.
The Stimuli for Emigration
Can attractive stimuli induce emigration? One possible interpretation of the mate search
hypothesis of King (1983) is that young are attracted from the natal site by the possibility of
mating. Another is that emigration might be stimulated by information as to the availability of
unoccupied habitat. Jones (1984) suggested that young Dipodomys spectabilis might be stimulated
to emigrate when they detected a mound made vacant by the death of an established individual.
Stickel (1979) recorded movement of 41 house mice from one field to another and interpreted
this as a response to the development of more favorable habitat in the new area rather than
deterioration in the old area. She did not speculate as to the means by which a distant, more
suitable, habitat was detected, although exploratory sallies across the intervening roadway might
have served the purpose.
Habitat deterioration and approach to the limits of a resource have been associated with
emigration in some instances. Movement could be the only alternative to immediate death in
kinds of habitat disturbance such as flooding (Aho and Kalela, 1966; Hansson, 1977). Freezing
has been observed to force muskrats out of small bodies of water (Errington, 1946, 1963). Such
factors have little relevance to the general problem of dispersal.
Uchmanski (1983) explored a model based on the assumption that animals emigrate when food
becomes inadequate to sustain them, and Grant (1978) hypothesized that emigration might be
stimulated by anticipated resource (nutrient) shortage. Full exploitation of the available food
supply triggered emigration of commensal Mus musculus (Strecker, 1954), but there was no
basis on which to conclude that movement was stimulated directly by hunger rather than
mediated by social interaction. Residents might not always emigrate in response to habitat
deterioration. Established individuals have been observed to remain on their home ranges despite
highly disruptive, or even devastating, habitat change (Friend, 1979; Getz, 1970).
Some data can be interpreted to indicate that emigration of virgin female Microtus ochrogaster
is stimulated by the absence of suitable male pheromones in the vicinity of their nest (see the
summary by Carter et al., 1986). In this species one or more male pheromones trigger sexual
maturation and estrus in young females. Emigration in search of such stimulation would be
analogous to the mate search hypothesis proposed by King (1983). However, Carter et al. (1986)
reported that pair-bonded resident males will not accept a transient female until she is activated,
suggesting that a virgin female may need to establish herself on an unoccupied area and either
await the arrival of a transient male or activate herself by sniffing scent marks left by nearby
male residents. The operation of this relationship with respect to emigration of female M.
ochrogaster is puzzling in the light of evidence that most surviving females breed within 30 m
of the natal site.
One fundamental assumption of the RFH is that inherently philopatric young are forced to
emigrate as a result of social stimuli. The RFH predictions are explicit: in other than exceptional
circumstances, such as catastrophic habitat deterioration, the proximate external stimuli for
emigration are social pressures exerted by dominant residents (usually parents) on subordinate
non-residents (usually their offspring). Stimuli received by potential emigrants are expected to
be related to competition for the requisites for reproduction, and to have a strong intrasexual
component, especially where competition for copulations is involved (males). Timing of stimuli
is expected to be related to the breeding season, and to be dependent on the maturation of the
offspring and on the residual reproductive value of the residents. The nature of the social pressure,
and its intensity, are expected to be influenced by altruism based on the relatedness of the
individuals exerting the pressure and those receiving that pressure. Interactions leading to em-
igration are expected to be intrafamilial, whether the family is matrilineal, nuclear, or extended.
80 Rodent Dispersal
Rodents fall into two categories with respect to parent-offspring relationships and the social
environment in which one might seek the proximate mechanisms of emigration. In one class
(seasonally polyestrous species), all except the juveniles of the last litter of the season must interact
with sexually active male and female residents. In this group, stimuli triggering emigration should
be directly discernible if observational difficulties can be overcome. In the other class (seasonally
monestrous species), encounters with reproductively active conspecifics do not take place until
the young are nearly a year old. The radically different contexts dictate separate discussions of
the topic of emigratory stimuli. ;
In seasonally polyestrous species, emigration occurs in both sexes and is associated with the
breeding season. Males are more likely to emigrate than females, transients are frequently younger
than residents, dominance is positively correlated with age and size, subordinate status and
emigration are frequently associated, social subordinates are often maturing young, and emi-
gration is associated with puberty (Baird and Birney, 1982a; Beacham, 1981; Christian, 1970;
Fairbairn, 1977a, 1978b; Gaines and McClenaghan, 1980; Myllymaki, 1977a; Myers and Krebs,
1971; Petticrew and Sadleir, 1974). Many authors have inferred that in these rodents emigration
is socially enforced (e.g, Beacham, 1980b; Burt, 1949; Christian, 1970, 1971; Cockburn et al.,
1981; Fairbairn, 1977a, 1977b; Krebs and Boonstra, 1978; Sadleir, 1965). Butler (1980) reported
that subordinates made up 95% of the “emigrants” crossing a water barrier in a laboratory
apparatus.
Does fighting induce emigration? Male emigration, in particular, is strongly correlated with
the breeding season. Aggressive behavior of males in many species increases prior to the initiation
of breeding (e.g., Flowerdew, 1978). Emigration at this time, as described by Fairbairn (1977b)
and Krebs and Boonstra (1978), is likely to be initiated by competition among males for mating
rights, and most emigrants should be mature males. To the extent that pre-season contests for
mating rights occur between non-relatives, they should be more likely to involve serious fighting.
Krebs and Boonstra (1978) found that males were more likely than females to disappear in this
pre-season stage, and that the rate of male disappearance, but not of female disappearance, was
positively correlated with the incidence of wounding.
Wounding studies are relevant to the questions of whether social pressure takes the form of
aggression, and whether parental aggression toward offspring is benign, as the RFH predicts.
Unfortunately, the majority of studies of wounding have attempted to establish a relationship
between population density and the frequency and intensity of aggression and are inconclusive
(Christian, 1971; Krebs, 1964; Lidicker, 1973; Rose, 1979; Rose and Gaines, 1976, 1981; Turner
and Iverson, 1973). These studies demonstrated that wounding was associated with reproductive
activity. Rose and Gaines (1976:48) stated that “voles of both sexes show substantially higher
levels of wounding during the periods of greatest reproductive activity. Christian (1970) reported
that immature male Microtus born late in the breeding season lacked scars, whereas mature
males of the same cohort bore scars. Nevertheless, wounding has not been directly correlated
with emigration.
The contention by Rose and Gaines (1976) and Rose (1979) that the highest levels of wounding
observed in their studies of M. ochrogaster were found after the breeding season seems inconsistent
with RFH predictions. Rose and Gaines noted that their results and those of Lidicker (1973) for
M. californicus suggested high wounding levels in winter. Wounding in M. ochrogaster did,
however, correlate with sexual competence in males (Rose and Gaines, 1976). Weanling females
lacked wounds, and thus were distinct from all other groups. Wounding among males was
associated with the transition into the heaviest weight class. Assuming these were the oldest
males, and noting the tendency for emigration to be delayed in this species, male aggression
might be related to a post-breeding replacement of old males. Gaines and Johnson (1984)
concluded, on the basis of regression analyses, that the ratio of transients to residents in M.
ochrogaster was negatively correlated with season and with male reproductive activity, but
positively correlated with the abundance of large males. Because late winter is the period of
peak reproduction for M. californicus, but not for M. ochrogaster, the Kansas and California
Testing RFH 81
situations are not parallel. The confusing evidence could reflect an inadequate allowance for the
unusual social structure and the bimodal breeding season in M. ochrogaster.
The greatest weakness of wounding studies is that the sex and relatedness of the individual
administering a wound and the circumstances (the site and the nature of the interaction) are
unknown. Wounding studies have produced only one consistent observation—wounding is related
to sexual maturity in males in the reproductive season (Gaines and McClenaghan, 1980). Because
wounding data fail to indicate whether the wounds were caused by males or females, and whether
wounds are acquired during courtship, mating, defense of territory against immigrants, emi-
gration, or expulsion of emigrants, wounding studies have so far shed little light on the nature
of the stimuli for emigration.
Emigratory stimuli given by resident females to offspring should follow a different seasonal
pattern than those originating from resident males, and should correlate with the cycle of estrus
and gestation, as well as with the reproductive state of female offspring. Females might drive
out young at the time a subsequent litter is born, or puberty or pregnancy of female offspring
could trigger maternal aggression. Viitala and Hoffmeyer (1985) speculated that most female
M. agrestis become pregnant while living on the maternal territory and emigrate while gravid.
The implication throughout the literature reviewed above is that emigration is stimulated by
aggressive interactions. However, an aggressive encounter and emigration can rarely if ever be
tied together. Despite the convergence of evidence and opinion pointing to emigration of sub-
ordinate young as a consequence of interaction with dominant adults I have been unable to find
any study in which individual episodes of stimulus and emigratory response have been given
detailed examination in polyestrous rodents. In particular, I have found no data sufficiently
precise to test the assumptions of the RFH.
In part, the inadequacy of the literature might exist because investigators have not focused
specifically on stimulus-response relationships leading to emigration. When this is done, several
possibilities will need to be considered. Emigration might be triggered by a single agonistic
interaction, a series of interactions, or a trend in the nature of interactions. When interactions
are between relatives, it could be advantageous if emigration were to be triggered in a single,
non-damaging, agonistic interaction. Some observations support a single-episode or key-inter-
action postulate. In arena-like spaces, social dominance and subordination may be established
in the first moments of a brief initial agonistic encounter (Anderson and Hill, 1965). Avoidance
is the behavioral response of mice defeated in arena encounters (Parmigiani et al., 1981). Thus,
emigration would be a likely outcome of one or a few aggressive interactions in an unenclosed
space. Butler (1980) observed a formerly territorial male Mus “emigrate” across a water barrier
in a laboratory enclosure within 10 min after the loss of a series of fights. Single encounters could
have persistent effects. Pituitary-adrenal response to defeat has been shown to be rapid (Archer,
1970; Bronson and Desjardins, 1971) and the behavioral and physiological responses to an initial
encounter are rarely reversed. Nevertheless, a key-interaction stimulus system would be difficult
to demonstrate in the field. If only one or a few agonistic interactions were required to tip the
scale in favor of emigration, the critical rare and ephemeral events might be easily overlooked.
An alternative to the key-interaction hypothesis is that emigration is induced by repeated, and
perhaps escalating, agonistic interactions. Although chances of observing one or more interactions
might be greater, the point at which emigration was elicited might be difficult to determine and
the differences in behavior toward emigrants and non-emigrants might be obscure.
If aggression leading to emigration is intrafamilial, the frequency of encounters, and of
aggression, need not be determined by crude density. Pearson (1960) monitored activity on
runway systems made by Microtus californicus and found that each system was used by a family
group. The frequency of encounters among individuals did not increase with increasing density
in the surrounding area. Indirect evidence obtained by Carroll and Getz (1976) supports Pearson’s
observation.
Abdication of home ranges by resident females is clearly an exception to the argument that
emigration is stimulated by the pressure of dominant residents on subordinate offspring. The
82 Rodent Dispersal
most conspicuous example of emigration under these circumstances has been reported by Price
et al. (1986). They observed that maternal female Tamiasciurus left their territories to offspring
and became transients, wandering until able to claim a vacant territory.
Establishment of a connection between emigration and a triggering stimulus should be easiest
in large-sized, diurnal species. Many such species, however, are seasonally monestrous, with life
history strategies centered on exploitation of abundant resources in a period of intense foraging
activity, followed by hibernation. In consequence, the relationships between emigration and
reproduction could be obscured. Holekamp (1984, 1986) has reviewed emigration in diurnal
sciurids. On the basis of an intensive study of the proximate causes of emigration in Spermophilus
beldingi, she proposed that emigration is internally motivated. S. beldingi exemplifies the extreme
life history pattern for seasonally monestrous species. As outlined by Holekamp (1986), Sherman
(1977, 1980, 1981), and Sherman and Morton (1984), emigration takes place in the following
context. The winter months are spent in hibernation. Above-ground activity takes place between
April and October, but all cohorts are not active throughout this period. Adult males are the
first to emerge from hibernation, and competitive interactions leading to a hierarchy that regulates
male mating success occurs at that time. Yearling males do not mate and thus do not participate
in this competition. Adult females are the next to emerge, and mate within a few days. Males
that succeed in mating disappear from the areas where they have mated and settle elsewhere.
Adult males that did not mate do not emigrate. Mortality of adult males in both groups is high
at this time.
Adult males enter hibernation when young are about 6 weeks old. Because young emerge
from their natal burrows at 25-28 days of age, which is after the successful males have departed,
there is no opportunity for interaction between males and their own offspring. Nevertheless,
sexual bias in emigration in S. beldingi is extreme with almost all females being philopatric and
almost all male young emigrating at about 10 weeks of age.
An interpretation of the dispersal biology of Belding’s ground squirrel requires two hypoth-
eses—one to explain the post-breeding emigration of successful males and the other to explain
the emigration of male young from an environment lacking active adult males, some 20 months
before they reach puberty. Holekamp (1986) specifically tested 10 hypotheses about proximate
mechanisms responsible for emigration of young males in their first summer: demand for food;
demand for nest sites; ectoparasite load; ontogenetic switch; intraspecific aggression directed at
juveniles; response thresholds to intraspecific aggression; conspecific avoidance of juveniles; ju-
venile avoidance of conspecifics; avoidance of nearest neighbors; and social facilitation. She
concluded that all except the “ontogenetic switch” hypothesis, which she visualized as a sex-
linked internal stimulus for emigration of young males, could be rejected. Holekamp’s study
raises two questions of special importance in the present context. Is the RFH applicable to S.
beldingi? Further consideration of both the biology of this species and the potential for an RFH
explanation for emigration in seasonally monestrous rodents is in order.
Emigration of young male S. beldingi begins 16 days after their emergence from their natal
burrows. In Holekamp’s populations, 74% of young males, but only 8% of young females, had
emigrated by 60 days of age. Male emigration appeared to be associated with attainment of a
body mass of 125-175 g. Because young males emigrate and most young females do not,
Holekamp’s search for a proximate cause of emigration was based primarily on comparison of
the stimulus environments of male and female young. Because she found no differences between
male and female young in mean levels of intraspecific interaction, Holekamp was led to postulate
a sex-specific internal trigger.
Holekamp did, however, record some significant differences in the experiences and behavior
of male and female young. Between the 7th and 9th weeks of age the frequency of chases
directed at males increased, while that directed at females decreased. During the 7th week of
life, males spent more time investigating non-natal burrows, and entered more of them. During
the 8th week males spent significantly more time climbing, and during the 8th and 9th weeks
males moved about at a significantly higher rate. The most interesting difference was derived
Testing RFH 83
from experiments designed to test response to interspecific threats. Between the 5th and 9th
week of life, male young re-emerged sooner from refuge burrows following fright reactions
induced by a simulated overflight by a predator. This observation calls attention to an important
point. The observations of intraspecific interaction dealt only with above-ground activity. Sub-
surface interactions could not be evaluated. Re-emergence of males following a surface fright
could reflect an inhospitable subsurface environment, and agonistic interactions below ground
could have caused male emigration.
Can the RFH provide a rationale for such subsurface antagonism (presumably on the part of
adult females or female siblings) and is there any evidence to support it? An hypothesis can be
built on the basis of maternal energy demands, female expectations as to further reproduction,
and observations on other species. Although Festa-Bianchet and King (1984) found no correlation
between dominance status and probability of disappearance of yearling S. columbianus, they
noted that the timing of yearling disappearance correlated with a peak in aggressiveness in
resident females. Yearling female marmots delayed emigration when adult females behaved
amicably toward them (Downhower and Armitage, 1981). Young male S. richardsonii were
philopatric only when maternal females failed to overwinter (Michener and Michener, 1973).
Adult female Belding’s ground squirrels have a mean longevity twice that of males, and have a
high probability of further reproduction at the site where they have produced a litter successfully.
If there is a social stimulus for emigration of male S. beldingi, it seems that it must originate
with the mother or female siblings. Rapid weight gain after lactation is especially critical for
survival of mothers and daughters. Both depend on retention of the foraging area to build fat
reserves required for overwinter survival. A significant finding in Holekamp’s study, suggesting
that there is competition for forage, is that the few females that did emigrate spent more time
foraging than did those that were philopatric. Export of young males might give a female and
her daughters an important competitive edge over other females.
Requirements of adult females might also influence the emigration of reproductively successful
adult males. Breeding success probably demands intensive energy expenditure. If adult males
have any chance of breeding in more than one season, emigration to avoid female competition
might be adaptive (an EFH explanation?), or be the best way to facilitate survival of presumptive
offspring (a male equivalent of female abdication in polyestrous rodents?).
There is ample opportunity for further studies designed to determine what stimuli induce
emigration, as well as for reinterpretation of data from previous studies on the basis of new
concepts and new data. Although there is support for the roles of dominance and social pressure
in inducing emigration, the picture is not sufficiently clear and detailed for evaluation of the
assumptions of the RFH. Future investigators might wish to evaluate relatedness in relation to
agonistic interaction, and consideration should be given to an examination of the hypothesis that
a single agonistic exchange between parent and offspring, moderated on the basis of their
relatedness, is sufficient stimulus for emigration.
Resident Behavior as a Cause of Emigration of Offspring
For most rodents the role of parents in the emigration of offspring is unclear. We can expect
parental strategies to differ with the parent’s sex and residual reproductive value, the sex and
potential competitive impact of philopatric offspring, and probable breeding success of the
offspring that emigrate. All of these factors vary seasonally, and all will vary with the reproductive
pattern of the species. Conclusions as to the role of parental behavior (particularly those made
under conditions of confinement) must be drawn with these considerations in mind.
Sadleir (1965) and Healey (1967) attributed disappearance of young Peromyscus maniculatus
from their natal sites during the breeding season largely to adult male aggression, but Howard
(1949) and King (1983) observed no parental aggression in association with emigration of young
Peromyscus. Halpin (1981) also found few instances of aggression between parents and offspring,
although the relevance of her laboratory findings to seasonally variable field environments and
84 Rodent Dispersal
adults of various ages is difficult to evaluate. Young P. maniculatus sometimes overwinter with
their parents (King, 1983; Mihok, 1979), and Fairbairn (1977a) noted a spring surge in numbers
of transient individuals, suggesting that delayed explusion of young may be characteristic of
some populations or cohorts.
The evidence is stronger for parentally-induced emigration in large, diurnal rodents. As
indicated above, the distance at which yearling male Spermophilus richardsonii settled was
correlated with overwinter survival of their mother (Michener and Michener, 1973). According
to Downhower and Armitage (1981), yearling male Marmota flaviventris are the primary re-
cipients of adult aggression, and harem males are more likely to initiate aggressive encounters
with yearling males (which generally emigrate) than with yearling females (which often do not).
Emigration of yearling males could not be correlated with the frequency of adult aggression,
but was positively correlated with build-up of energy reserves. The timing of emigration of
yearling females correlated positively with high rates of aggression among female peers and was
associated with above-ground appearance of young of the year. Whether or not yearling females
emigrated appeared to be independent of whether or not young appeared. In Microcavia, adults
of both sexes are aggressive toward adolescent males. Adult females may drive their young away
from the home bush at the time a new litter is about to be born, although at least some of the
young are allowed to return later (Rood, 1970).
Resident Male Aggression and the Export of Offspring
The interests of male and female residents could conflict with respect to expulsion of young.
In marmots, harems often consist of two or more matrilines. Matrilineal success decreases with
harem size, whereas paternal fitness increases (Armitage, 1986b). Armitage (1984) found no
evidence that male marmots inhibited recruitment of yearling daughters into their harems.
Harem males might gain by retention of female young, but harem females could lose, especially
if retention is indiscriminate among matrilines. Females could also lose if resident males dis-
criminate harshly against sons. Although Rood (1970) attributed emigration of adolescent Mi-
crocavia to aggressiveness of adults of both sexes, female adolescents were not expelled by resident
males. These observations are in accord with a general lack of evidence that resident male
behavior is such as to reduce the likelihood of father-daughter matings.
If “pre-saturation dispersers’” (Grant, 1978; Lidicker, 1975) are largely pubertal males, their
emigration might well be due to pressure from adult male residents, but it is difficult to reach
a clear conclusion as to the role of males in expelling sons because, in most studies, emigrants
have not been identified with sufficient assurance and consistency, or categorized by sex and
season. Myllymaki (1977a) recorded that in a large enclosure young male Microtus agrestis
belonging to the first two spring-born cohorts were “badly treated” by dominant overwintered
males and sought corners rarely frequented by the dominant males. Jannett (1981a) observed
that only young males in which testes had not descended were able to persist in dense M.
montanus populations, but he had no direct evidence that young males were expelled after their
testes descended. In most other field studies evidence that males become intolerant of sons around
the time the latter reach puberty, and that parental aggression results in filial emigration, is even
more difficult to pin down.
Gaines and Johnson (1984) applied regression analyses to data obtained in studies of M.
ochrogaster and found that as the proportion of reproductively active adult males increased, the
ratios of apparently transient adult females, subadult males, and subadult females to residents
decreased. Thus male reproductive activity was a negative predictor of transient abundance.
The negative correlation between reproductive activity of resident males and disappearance of
subadult males appears contrary to the RFH, but the data are confusing due to the criteria used
to define the various categories, and seasonal effects are difficult to evaluate in the analysis.
The literature also fails to provide any particular relationship between emigration of male
offspring and their reproductive condition. According to Krohne et al. (1984), most male Pero-
Testing RFH 85
myscus leucopus making long one-way movements had undescended testes; those that successfully
dispersed were non-scrotal at the time they emigrated, but became scrotal after settling in a
new area. Fairbairn (1978a) followed Sadleir (1965) and Healey (1967) in attributing high juvenile
disappearance rates in Peromyscus to resident male aggression. Nadeau et al. (1981) came to a
similar conclusion. Fairbairn (1978a) believed, despite a lack of direct observation of interactions
in the field and without discriminating with respect to sex of offspring, that male aggressiveness
caused death of most young P. maniculatus born during the period that she designated as the
main breeding season. She did not speculate as to the evolutionary process that would lead males
to kill or cause death of their own offspring. Wolff and Lundy (1985) reported avoidance but
no overt aggression in encounters of same-sex, adult-juvenile pairs staged on the home ranges
of resident adult P. leucopus. Savidge (1974) found that male P. maniculatus were tolerant of
young of both sexes in the laboratory. Mihok (1979) reported that in northern Alberta, young
Peromyscus cohabited with parental pairs over the first winter. King (1983) observed that
association of young Peromyscus with their fathers increased at the end of the breeding season.
Taitt (1981) reported a predominance of males among recruits to populations of P. maniculatus
during the non-breeding period. More detailed studies are needed to resolve the differences
among these studies.
Gipps et al. (1981) failed to influence density in Microtus townsendii significantly by treatment
of young males with testosterone implants (which were expected to increase male aggressiveness),
or with scopolamine (which was expected to reduce it). The scopolamine did appear to slow the
decline in numbers of males at the start of the breeding season. Boonstra (1977b) found that
experimental reduction of density of M. townsendii did not affect male disappearance rates (i.e.,
neither survival nor emigration of males appeared to be density-dependent), but he did observe
that young males became sexually mature at a lighter weight on grids from which adult males
were removed. Boonstra and Rodd (1983) reported that removal of adult male Microtus had
little effect on the persistence of other sex-age cohorts on open experimental plots. Pfeifer (1982b)
indicated that juvenile male Spermophilus elegans appeared to avoid adult males, but she did
not observe agonistic interactions that would suggest active expulsion of young by the adult
males.
The literature does not presently provide a satisfactory basis for evaluation of male roles in
the emigration of their sons and daughters. We need studies in which such factors as the season,
the seasonal cohort, the sexual state of adults and young, the residual reproductive value of the
male parent, and the degree of genetic relatedness are precisely specified. It is especially important
that these studies be designed in such a way that the relevance of the results to natural situations
is unequivocal. Although the general trend of the evidence appears to support the hypothesis
that males expel pubertal sons and are tolerant of daughters, the conclusion that this is the case
must remain tentative at present.
Resident Female Aggression and the Export of Offspring
Kalela et al. (1961) attributed the early male migration from summer to winter habitat in
Lemmus lemmus to female aggression. Redfield et al. (1978a) found that removal of female
Microtus oregoni increased persistence of young, but that removal of males had no effect.
Experimental alteration of sex ratios in populations of M. townsendii also showed that recruitment
of young was inversely related to female density (Redfield et al., 1978b), and that sex ratios
biased in favor of adult females reduced persistence and recruitment of juveniles. Young female
Clethrionomys gapperi occupied areas not claimed by overwintered females, but moved into
the territories of the latter when death of residents created vacancies (Perrin, 1979).
Because so much effort has been concentrated on male aggression, evidence as to the influence
of females on emigration is scattered. Female aggression toward potential emigrants is likely to
be affected by the hormonal cycles associated with gestation and lactation, and by social cir-
cumstances. Aggressiveness of female Peromyscus leucopus increases with dosage of progesterone
86 Rodent Dispersal
(Gleason et al., 1979). Gray (1979) found that in ICR mice, female aggressiveness toward juveniles
peaked during the first 2 weeks postpartum. Virgin females also attacked juveniles, and virgins
housed in groups were more aggressive toward juveniles than were those kept in isolation.
If female aggression is based on anticipated resource demands, we might expect females to
expel young in association with the birth of a succeeding litter. Female Chinese hamsters (Cri-
cetulus griseus) with new litters in a laboratory enclosure became aggressive toward both un-
familiar young and their own older young (Dasser, 1981). Festa-Bianchet and King (1984) noted
that the peak in adult female aggression in Columbian ground squirrels came just prior to the
time when yearlings disappeared from the colony and that prior to emigration the young shifted
the sites of their activities so as to avoid female aggression. In a laboratory environment, ag-
gressiveness of newly parturient females was associated with movement of young P. maniculatus
across an electrified barrier to an adjacent cage (Savidge, 1974).
When female Dipodomys spectabilis abdicated their home mounds to offspring, the settlers
were predominantly female. When the female died, the offspring settling on the home mound
were predominantly male (Jones, 1986). Such observations support the notion that females, as
well as males, may expel male offspring.
If female competition is resource-based, behavior of resident females may be linked to emi-
gration through population responses to food shortage. The RFH anticipation that female-induced
emigration should be triggered by food shortage is partially supported. Myllymaki (1977a)
attributed increased emigration by voles to decreased availability of food and to aggressive
behavior of females toward offspring midway in the reproductive season.
Desy and Thompson (1983) increased persistence of juvenile Microtus pennsylvanicus on plots
by addition of high quality food, and Cole and Batzli (1979) found that supplemental food
increased the proportion of juveniles overwintering in M. ochrogaster. Gilbert and Krebs (1981)
induced both increased juvenile recruitment and immigration in unconfined populations of
Peromyscus and Clethrionomys by supplying high quality food (sunflower seeds). However,
Ford and Pitelka (1984) concluded that persistence of young was not determined by resource
availability. They found that food supplementation in the spring lowered persistence of young
M. californicus in the population.
In an imaginative experiment, Smith et al. (1984) compared heterozygote frequency on food-
supplemented and non-supplemented grids. Population density was higher with food supplements
and heterozygote frequency was lower. This result was interpreted as indicative of selection for
hybrid vigor on the grids with less food. An equally tenable hypothesis is that decreased turnover
and increased inbreeding due to retention of offspring explained the low heterozygote frequency
on the food-supplemented plots.
The most important and conclusive pair of studies on the relationship between emigration
and food resources seem to have been largely forgotten. In confined populations of Mus, female
reproduction was suppressed by food shortage (Strecker and Emlen, 1953), but in an unconfined
population there was no curtailment of reproduction, and emigration began when food was
unavailable (Strecker, 1954). Strecker’s study unequivocally identified emigration as related to
density and implicated emigration and free egress as the essential elements in behavioral responses
that limited density in relation to a resource base, although the data do not tell us whether the
emigrants responded directly to food shortage or to pressure from residents.
Provision of supplemental food enabled Sheppe (1965) to reduce emigration from populations
of P. leucopus experimentally introduced on small islands. Pokki (1981) observed that movement
of M. agrestis between islands peaked in conjunction with vegetation decline.
Following a study on the relationship of forage quality to emigration in voles, Grant (1978)
argued that although elements such as Na, N, or P might have been insufficient, initiation of
emigration did not coincide with a sharp decrease in nutrient content of the grass. His calculated
requirements were, however, based on young males and thus failed to account for female
requirements during pregnancy and lactation. Further, each female should adjust behavior on
the basis of food quality within her own home range, and because individual ranges can differ
Testing RFH 87
greatly in quality (Cockburn and Lidicker, 1983), a clear-cut relationship such as the one Grant
tested would be unlikely.
Madison et al. (1984) regarded the tendency of extended families of M. pennsylvanicus in an
enclosure to retain male offspring selectively and exclude female offspring as an extension of
resource competition by the breeding females. The result was retention of familiar males, es-
pecially sons, at times when resource supplies were declining but resource requirements remained
high. However, if a mother expels her young in order to preserve resources for her present or
future investment, it might be predicted that export of daughters will sometimes take precedence
over export of sons. Any bias toward export of daughters would be most likely to occur as
daughters approach puberty or parturition and are likely to use more of the available resources.
This might explain the observations of Gaines et al. (1979a) that subadult females captured on
a removal plot were more likely to be in breeding condition than females of equivalent weight
captured on an adjacent control plot. Myers (1974) reported, similarly, that female house mice
that emigrated were more likely to have perforate vaginae than those remaining on the natal
grid. Gaines and Johnson (1984) found that the ratio of females of adult and subadult weight
encountered on a removal plot to density on nearby control plots increased as the percentage of
females in breeding condition on the control plots increased. The implication is that expulsion
of female voles into the transient population increased with the proportion of resident females
that were reproductively active. Although this may be indicative of a female role in expelling
female young, it is difficult to exclude other variables or to demonstrate a cause-and-effect
relationship on the basis of the available data. Downhower and Armitage (1981) stated that
aggressiveness of female marmots was greater in larger harems, and the increase in aggressiveness
along the harem-size gradient was directed more toward female yearlings than toward male
yearlings.
By experimentally reducing density of resident M. townsendii, Boonstra (1977a) was able to
lower female disappearance rates. Boonstra (1984) noted considerable behavioral variation among
female M. pennsylvanicus toward young, but provided no indication as to the cause. Mihok
(1981) stated that in arena encounters female Clethrionomys gapperi were most aggressive
toward female young of the year. Relatedness was not assessed in either study and, additionally,
their relevance to field situations is unclear. Contrary to the interpretation of their results by
Boonstra and Rodd (1983), there is no clear case for a consistent effect of removal of adult female
Microtus on persistence of younger females on their grids during the breeding season because
the effect varied between years.
The ability of adult females to suppress sexual activity of juvenile or adult female conspecifics
pheromonally has been demonstrated in various species in the laboratory (Batzli et al., 1977;
Champlin, 1971; Drickamer, 1974; Whitten, 1959). Because it serves to limit demand on resources
by restricting recruitment to the breeding population (Getz et al., 1983), it might be an alternative
to forced emigration of daughters. Gilbert et al. (1986) reported that when all adult female
Clethrionomys rufocanus were removed from two areas after the weaning of the first litter of
the season, female young of the year bred on these female-removal grids, but not on control or
on total-removal grids. These results suggest that the function of reproductive suppression was
not to prevent inbreeding or to stimulate emigration of young so that they might reproduce, but
instead to prevent premature reproduction of female young and thus prevent philopatric daugh-
ters from competing with maternal females. Immigrants to the female-removal plots in this
experiment were primarily young of the year. Massey and Vandenbergh (1980) found that in
“island” populations of Mus only females living at high densities produced urine that was capable
of inhibiting juvenile female maturation. Coppola and Vandenbergh (1987) induced secretion
of a urinary pheromone that had the same effect by introducing transient females.
Bujalska (1970, 1971), Mihok (1979), and Perrin (1979, 1981) have all observed that the number
of reproductively active female Clethrionomys remained relatively constant while overall density
on their study plots varied more widely. Bujalska (1970, 1971), studying C. glareolus on a small
island, demonstrated that breeding was dominated by over-wintered females, and that these
88 Rodent Dispersal
were spaced evenly throughout the available habitat. The number of sexually inactive females
varied considerably. Young females from the spring cohorts bred only when they were able to
occupy a vacancy created by the disappearance of an older breeding female. Removal of females
born in early cohorts increased the proportion of females born in the later cohorts breeding in
the year of their births (Bujalska, 1973). Bondrup-Nielsen (1986) also demonstrated that removal
of adult female Clethrionomys was followed by maturation of previously suppressed young
females, and Armitage (1986b) reported that the presence of older female marmots reduced the
chances that 2-year-old females would breed.
Myllymaki (1977a) attributed the tendency of female Microtus agrestis to leave their newly
weaned litters in the nest and shift their own home ranges just before the birth of a new litter
to a release of maternal bonds and a spontaneous tendency to emigrate. Contrary to the view
that recruitment of young is strongly influenced by the density of females (Boonstra, 1978,
Redfield et al., 1978a, 1978b; Taitt, 1981; Taitt and Krebs, 1982, 1983), he concluded that female
territoriality had little or no effect on dispersal. Abdication of all or part of the maternal range
by females that have weaned their young might represent an alternative outlet for maternal
aggressiveness.
Direct evidence that young emigrate in response to female aggression is hard to find. Female
red squirrels (Tamiasciurus) have been observed to drive young out of their territories at weaning
(Rusch and Reeder, 1978). Randall (1984) observed female Dipodomys spectabilis chasing female
offspring away from the natal mound and driving them away again when they attempted to
return. Yahner (1978) believed that young Tamias left voluntarily. He stated that he saw no
evidence that maternal females expelled their young, but he observed that young returning to
the natal site after several days were attacked by their mothers. In the two instances where
young settled at the natal site, the maternal female had moved or disappeared.
Increased tolerance of offspring by females has been observed as the breeding season ends
and residual reproductive value of the breeding population is exhausted (Jannett, 1978; Perrin,
1979; Viitala, 1977). Decline in the tendency of young to emigrate as the end of the breeding
season arrives has been noted in Apodemus (Flowerdew, 1978; Watts, 1970), Mus (Naumov,
1940), and Peromyscus (Mihok, 1979), but a direct connection between increased female tolerance
and philopatry of young at this season has yet to be established.
Viewing the evidence, there is much to be learned regarding any role of resident females in
regulating dispersal. Most of the recent studies do support the generalizations that females are
intolerant toward unfamiliar individuals of both sexes, that female territoriality opposes settlement
of transients, and that female residents can inhibit immigration of sexually mature female
conspecifics, but the picture of the role of females in opposing immigration is still far from
definitive. Female resource competition provides a basis on which expulsion of offspring might
function, but direct evidence that females actively expel either male or female offspring is scant.
Although the importance of female behavior is being increasingly recognized, more detailed
studies on the role of females in emigration of offspring are needed. The present trend favors
the RFH prediction that female behavior will have a significant effect on emigration as it relates
to density, and will be more influential than male behavior in limiting density increase. Never-
theless, the opinion of such careful workers as Myllymaki (1977a:561) that “it is possible to
dispense with the theory that female territoriality and aggressiveness are major demographic
forces’ cannot be ignored.
Responses of Young to Resident Pressure
There is little evidence that in unconfined populations young are likely to displace parents or
other residents through confrontation or other forms of agonistic behavior. Young marmots always
lose agonistic encounters with adults (Armitage and Johns, 1982). Evicted individuals sometimes
establish themselves near, but out of routine contact with, natal or non-natal colonies. In arena
encounters young Microtus ochrogaster that had not had an opportunity to establish pair-bonds
rarely initiated agonistic interactions (Getz et al., 1981). Metzgar (1971) observed that young
Testing RFH 89
Peromyscus leucopus tended to settle in the interstices between resident home ranges, or to take
over ranges vacated by residents. Downhower and Armitage (1981) noted that yearling female
marmots delayed emigration when adult aggression was low.
The two physical responses available to young in the face of parental pressure are emigration
or adoption of “peripheral” status but, if adult pressure is significantly dependent on the state
of development of offspring, delayed maturity might serve as an alternative. From the point of
view of the offspring, delayed maturity in response to adult pheromones could be adaptive if it
staves off pressure to emigrate and thereby facilitates philopatry.
In most seasonally polyestrous species, persistence of young of both sexes at the natal site
probably increases with the end of breeding by residents, although few authors have examined
the point critically. It has been specifically reported in Apodemus sylvaticus by Flowerdew
(1978). Overwinter delay in emigration of males from the last litter of the season has been
observed in Microtus townsendii (Beacham, 1979b) and M. montanus (Jannett, 1978), and
reported for Mus by Naumov (1940).
Although the interplay of adult pheromones and juvenile response might also reduce the
possibility of inbreeding (Rissman and Johnston, 1985; Rissman et al., 1984), the competition-
suppression and emigration-avoidance explanations are obviously favored when the relationship
is intrasexual. The inbreeding-avoidance explanation is favored when maternal cues are most
effective in delaying male maturity (e.g., in Microtus californicus as reported by Rissman et al.,
1984). The fact that in experimental populations the initial stocks can inbreed freely, and delayed
maturity becomes evident only when crowding results from lack of egress (e.g., the “growing”
house mouse populations of Brown, 1953), favors the competition-explanation over the inbreed-
ing-explanation, but the two are not mutually exclusive in most situations.
Available evidence supports the assumption that juveniles generally fare best if they avoid
challenging residents. Terman (1961) conducted experimental releases of laboratory-reared Pero-
myscus maniculatus in large field enclosures and concluded that the ultimate pattern of dispersion
was best explained on the basis of avoidance of same-sex residents by the settlers rather than
aggressive defense by the residents. Van Horne (1981) concluded that there was a tendency for
young Peromyscus to be displaced to less favorable niche space. She observed that when density
was high, younger individuals consumed less of certain preferred foods and occupied habitats
with less cover. Tardiff and Gray (1978) reported that immigrants sampled a wider range of
foods than residents.
The assumption of the RFH that the options available to offspring are determined by the
behavior of residents is supported by a variety of observations. If young become transient,
encounters with residents, or with indications of occupancy such as feces, urine, or other scent
marks, could induce avoidance responses and young could be stimulated to continue wandering.
Avoidance could therefore be an important factor in dispersal distance. Neither adults nor young
should be expected to be uniform in their behavior, and both stimulus and response are likely
to vary with genotype and experience (Armitage, 1986a). Nevertheless, patterns can be expected.
There is ample opportunity for direct studies of the behavior of transients in response to runways,
scent marks, and encounters with residents under actual or simulated field conditions.
Responses of Male Offspring
Downhower and Armitage (1981) observed that young male yellow-bellied marmots were
subject to both maternal and paternal pressure. Although it remains to be demonstrated that this
is true in most species, the majority of young males probably emigrate. In studies to date, males
have predominated among presumed emigrants and disappearance rates of young males have
generally been higher than those of female siblings (Dice and Howard, 1951; Dobson, 1981,
1982; Festa-Bianchet and King, 1984; Gaines et al., 1979b; Gaines and McClenaghan, 1980;
McLean, 1982; Myers and Krebs, 1971; Pfeifer, 1982b; Sherman, 1977; and others), and the
proportion of young males known to establish near the natal site lower than that of their female
siblings (Holekamp et al., 1984; McLean, 1982; Schwartz and Armitage, 1980). Young male
90 Rodent Dispersal
emigrants settle at greater distances from their natal sites than do their sisters (Dice and Howard,
1951; Dobson, 1981; Holmes and Sherman, 1982; McLean, 1982; Michener, 1981, 1984; Pfeifer,
1982b).
There is evidence that as young males enter puberty they avoid adult males. Juvenile male
hamsters in a laboratory enclosure showed preference for unoccupied nest sites over those
occupied by adults of either sex (Dasser, 1981). Viitala and Hoffmeyer (1985) marked traps with
hexadecylacetate, a substance present in the preputial gland secretion of dominant adult males,
and found that subadult male and subordinate adult male Clethrionomys glareolus avoided
these traps. Measurement of aggression in arena encounters might be misleading with respect
to responses of juveniles, especially if a juvenile resorts to aggression when means of avoidance
are unavailable. This might explain the observation of Perrin (1981), who reported that in C.
gapperi male young of the year were the most aggressive cohort in arena encounters staged
between late June and September.
The correlation in males between sexual maturity and tendency to emigrate could result
entirely from internal mechanisms, or from a response by residents to evidence of maturity.
Holekamp et al. (1984) postulated that perinatal androgen levels might explain male-biased
emigration rates in ground squirrels, but provided no direct evidence to support the fundamental
assumption that male emigration was internally induced. In some ground squirrels emigration
of young males can occur well before sexual maturity (Holmes and Sherman, 1982). More
commonly, young ground squirrel males leave the natal site at or shortly before sexual maturation
(Armitage and Johns, 1982; Pfeifer, 1982b), and departure is associated with aggressive inter-
actions with paternal (Armitage, 1974; Christian, 1970) or fraternal (Pfeifer, 1982b) males.
In some species of Spermophilus, fathers depart before young emerge from natal burrows and
therefore there is little probability of father-son contact (Holekamp, 1986; Michener, 1979). In
other species, disappearance of the male parent reduces the probability that sons will emigrate.
Armitage (1974) concluded that the presence of an adult male in a colony of marmots was a
prerequisite for yearling male emigration. Svendsen (1980) observed that following the death of
the father, a young male beaver did not emigrate but instead settled in the natal lodge and was
accepted as a mate by his mother. Correlation between absence of a male parent and failure of
young males to emigrate is contrary to the argument that emigration is selected on the basis of
incest avoidance.
If sexual maturity triggers external pressures (or internal drives) toward emigration there
should be a correlation between transiency and sexual status at the appropriate seasons. Data
are variable as to sexual maturity of transient males. Transient male Clethrionomys glareolus
were usually sexually mature (Kozakiewicz, 1976), but Krohne et al. (1984) found that most male
Peromyscus leucopus that emigrated had abdominal testes. Forty percent of subadult Microtus
townsendii of both sexes identified as emigrants by Beacham (1981) were in breeding condition,
compared with only 15% of non-emigrants. Beacham suggested that sexual maturity at a low
body weight predisposed animals to emigrate. Male M. townsendii taken in pitfall traps were
more likely to have descended testes than were males of equal or greater weight caught in live
traps (Beacham and Krebs, 1980).
There are broad associations among male puberty, emigration of male young, higher probability
of males emigrating relative to their sisters, and the presence of sexually active adult males. In
many species sexual maturity occurs later in males than in their female siblings (Frank, 1957;
Holmes and Sherman, 1982; Koponen, 1970; Myllymaki, 1977a; Schwarz et al., 1964; Stenseth
et al., 1977). Busher and Jenkins (1985) reported that yearling male Castor canadensis behaved
less like adult males than did their female siblings. Stoddart (1973) noted that until sexual maturity
the tail-gland secretions of young male Apodemus show chromatographic patterns resembling
those of the mother. Assuming identification of sex and status are olfactory, this could be an
example of chemical camouflage offering protection from emigratory pressures. Delayed emer-
gence by yearling male ground squirrels until after the mating season is over (Slade and Balph,
1974) might have a similar effect. However, Porter and Dueser (1986) were unable to demonstrate
Testing RFH 91
suppression of male growth or maturity in Microtus when the proportion of large resident males
in the population was high, nor early maturity when the proportion of adult males was low.
There is little evidence to suggest that young males challenge male adults for the right to
remain on the natal site. If sexual maturity of male offspring triggers agonistic behavior of
resident males, delay in sexual maturity may avoid or delay forced emigration and thereby
facilitate philopatry. It may be to the advantage of both fathers and their sons if young males
postpone emigration when they have little chance of success (e.g., Rissman et al., 1984).
Pheromones produced by adult male Peromyscus sp. have been shown to retard the devel-
opment of the testes and seminal vesicles in young (Lawton and Whitsett, 1979). On the other
hand, one or more pheromones carried in the urine of breeding females can accelerate sexual
maturation in young males (Drickamer, 1984). This could either increase the probability that
male offspring would be expelled by resident males or make young males available as mates for
maternal females.
In polyestrous species, adult male pressure on young males is likely to be continuously high
until near the end of the breeding season. Turner and Iverson (1973) speculated that young male
M. pennsylvanicus never establish home ranges during the breeding season of their birth. Overall,
there is much circumstantial evidence to support the RFH assumption that emigration of young
males occurs in the course of puberty in response to pressure of residents, but there is as yet no
definitive picture of the stimulus-response system that leads to emigration or philopatry in young
males of any species. Competition among young males is another possible factor but fraternal
relationships have received little study.
Responses of Female Offspring
Young females behave as the RFH predicts. Dispersal distances of female ground squirrels
were less than those of males in most studies (e.g., McLean, 1982). Exceptions (Holekamp, 1984)
and observations that females are in the majority among transients (Dobson, 1981; Jordan, 1971)
are rare. Dice and Howard (1951) reported the average distance between natal site and breeding
site for female Peromyscus that dispersed was 57 m, as opposed to 121 m for males.
Response to paternal aggression is not a factor in emigration of female young in Marmota
flaviventris (Armitage, 1974). Unfortunately data about this are not available for other species.
Emigration of young females is a response to maternal aggression in Spermophilus elegans
(Pfeifer, 1982b). Aggression by, or avoidance of, female residents other than the mother also
might lead either to emigration or continued transiency in female young. In laboratory enclosures
juvenile female hamsters avoided nest sites of adult females but did not avoid those occupied
by adult males (Dasser, 1981).
The combination of female nepotism and philopatry might produce a lag effect in emigration
of young females. Gaines and Johnson (1984) found that of all sex-age cohorts of Microtus
ochrogaster encountered on a removal grid, only subadult females differed in comparison with
trapping results from a control grid.
As noted above, female young can be inhibited reproductively when kept in continuous close
confinement with female kin in the laboratory (Batzli et al., 1977; Drickamer, 1974; Richmond
and Stehn, 1976) and by forced exposure to maternal pheromones in the wild (Getz et al., 1983;
Massey and Vandenbergh, 1980). In some cases the inhibitory effect on female young of pher-
omones produced by adult females appears to be dependent on physical contact (Batzli et al.,
1977; Terman, 1980). It is not certain that contact outside of captivity would be adequate to
suppress sexual maturation, but Saitoh (1981) reported that confinement with overwintered
females in outdoor enclosures delayed maturation of spring-born female Clethrionomys rufo-
canus. Removal of adult female C. rutilus (Gilbert et al., 1986) from an unconfined population,
and of adult female C. gapperi from both confined and unconfined populations (Bondrup- Nielsen,
1986), was followed by maturation of young females that otherwise probably would not have
matured at that time. Although removal of overwintered females in spring stimulated breeding
in young females, removal of overwintered adult females in fall had no effect on young at a
92 Rodent Dispersal
time when breeding was continuing in the overwintered adults (Bondrup-Nielsen and Ims, 1986).
Bujalska (1973) found that removal of members of both the overwintered and first spring cohorts
in an island population of C. glareolus increased reproductive activity of females of the subsequent
summer cohort.
Many authors have noted an inverse relationship between rate of sexual maturation in females
and population density, and have inferred that delayed sexual maturation is a density-limiting
response (e.g., Bondrup-Nielsen and Karlsson, 1985; and references cited therein). In most such
instances, crude density peaks at the end of the breeding season, when delayed sexual maturity
would be anticipated as a seasonal response. The density relationship therefore may be incidental
to strategies specified by the RFH.
A key question in the present context is whether inhibition of sexual maturity acts as a stimulus
to emigration or a mechanism to delay emigration. There are a number of possible ways in
which delayed sexual maturity of young females could be adaptive for parents or offspring (e.g.,
Frogner, 1980; Stearns and Crandall, 1981a, 1981b). Depending on season, population density
and sex-age composition, and the like, delayed sexual maturity in female young could have one
or more of the following effects: 1) limit intra-familial competition; 2) retain young females as
helpers to care for younger siblings; 3) optimize the timing of emigration of female offspring;
4) reduce the probability of incestuous matings; 5) conserve young females in the home range
for future matings; 6) force females to emigrate in order to breed; 7) be a means by which young
females avoid emigration, thereby facilitating philopatry and continuation of matrilines. The
available data support most of these possibilities.
If a virgin female Microtus ochrogaster is caged with a reproductively active adult female,
male-induced reproductive activation is suppressed (Getz et al., 1983). Such inhibition of maturity
in female young may function to alleviate intrasexual competition. This is supported by the
parallel to Bujalska’s studies of Clethrionomys glareolus (Bujalska, 1970, 1971, 1973), in which
suppression of reproduction in young females living within the home range of a reproductively
active female seemed to function primarily to regulate the number of breeding females. Viitala
and Hoffmeyer (1985) suggested that pheromones produced by adult females could have the
effect of limiting female competition in C. rufocanus.
Because older offspring might contribute substantially to the care of nestling M. ochrogaster
(Getz and Carter, 1980; Getz et al., 1981; Thomas and Birney, 1979), the concept of retention
of young as helpers is also supported. Midsummer droughts bring about a midsummer lull in
reproduction over much of the range of M. ochrogaster. At this season, delayed maturity of
female young could serve to prevent emigration at an unfavorable time.
Because females fail to become sexually activated by familiar males, and in this pair-bonded
species familiar males are likely to be related (fathers or brothers), it is also logical to suggest
that delayed sexual maturity evolved as a means of preventing inbreeding (McGuire and Getz,
1981). The fact that pre-pubertal confinement of non-related adult-young pairs produces the
same inhibition as confinement with relatives (Gavish et al., 1984) weakens the “incest taboo”
argument, but does not negate it. Agren (1984a) found that in Meriones unguiculatus, as in
Microtus ochrogaster, sexual maturity of young females is inhibited as effectively through
constant close contact with familiar non-relatives as with relatives.
Is delayed sexual maturity in females a spur to emigration, or a means by which emigration
of young females is delayed or avoided? Familiarity barriers to female activation and mating
erode when the familiar animals are temporarily separated (Dewsbury, 1982c; Gavish et al.,
1984; Hill, 1974; Huck and Banks, 1979; McGuire and Getz, 1981; Porter and Wyrick, 1979;
Richmond and Stehn, 1976) and the question of whether contact is constant enough, and fa-
miliarity sufficiently strong, to prevent female maturity in the wild has yet to be answered.
Although it appears that those female M. ochrogaster that emigrate will be the first to enter
estrus, there is no evidence that absence of estrus is a stimulus to emigration. Further, it is not
known if emigration results in an increased rate of sexual maturation. In laboratory arena tests,
mated male M. ochrogaster were aggressive toward unfamiliar virgin females. It is therefore
Testing RFH 93
unlikely that transient females would be activated by, or establish breeding relationships with,
pair-bonded resident males (Getz and Carter, 1980; Getz et al., 1981).
In seasonally polyestrous species, patterns of growth and maturation vary markedly with the
time of birth (Anderson, 1970; Gyug and Millar, 1981; Martinet, 1967; Reichstein, 1964; Schwarz
et al., 1964). Failure of female offspring to emigrate in the latter part of the breeding season
has been observed frequently (Batzli and Pitelka, 1971; Beacham, 1979b; Lidicker, 1980; Mihok,
1979; Myllymaki, 1977a), and as pointed out above, optimal dispersal strategies for both parents
and female young could be served by delayed maturation at that time. McClintock (1983)
suggested that delay in sexual maturation of young female voles until they are able to claim a
territory, as observed by Bujalska (1970, 1971, 1973), is an adaptive response on the part of the
young in that it serves to delay reproduction until adequate resources are available.
If transient females have a higher probability of immigrating than do their male siblings,
activation by unfamiliar males could assist in this process. Female transients penetrate established
populations (immigrate) more frequently than do males in at least some species (Anderson, 1965;
Eibl-Eibesfeldt, 1950; Redfield et al., 1978b). For the present, the conclusion must be that there
is no evidence that juvenile females in unrestricted situations normally respond to maternal
pheromones or “excess” familiarity with male relatives by delaying sexual maturity. Further
experiments like those of Massey and Vandenbergh (1980) are needed to resolve the question.
In summary, young females are more likely to settle philopatrically than are their brothers.
In a few cases it is reasonably clear that maternal aggression is responsible for emigration of
young females. Even so, little is known about the proximate stimuli and responses that determine
whether a young female will emigrate or settle at its natal site. It appears that young females
are unlikely to experience agonistic interactions with their father; mothers tend to behave in an
affiliative or nepotistic manner unless stressed by resource shortages. Maternal aggression, if any,
is likely to be associated with pregnancy or parturition. Competition between sisters might be
similarly triggered and act as an additional source of pressure to emigrate in some species. Sexual
maturation in females of at least some species can be delayed by either maternal pheromones
or insufficient contact with pheromones of mature males, but there are many possible functions
for such inhibition and their relationship to emigration and other aspects of dispersal remains
problematical.
The Confinement Syndrome: Consequences of Lack of Egress
If some individuals are behaving in a way that has evolved because it causes others to emigrate,
and emigration is impossible due to physical barriers, the frustration of the normal processes can
be expected to lead to abnormal consequences for both those exerting the pressure and those
receiving it. Beginning in the 1950’s, studies of confined populations of mice, rats, and voles
have consistently reported results that seem counterproductive in evolutionary terms and are
not readily interpretable except as abnormalities associated with pressure on potential emigrants
combined with lack of egress.
The RFH predicts that when egress is blocked, pathological behavioral or physiological effects,
or both, should be most immediate and most extreme with respect to the potential emigrants.
Established individuals should be the last and least affected as density increases. The effects of
confinement therefore should provide clues to the identity of potential emigrants and to the
mechanisms that normally induce emigration.
The classic confinement syndrome, in which a confined population grows to a high density,
following which growth is terminated by behavioral and physiological abnormality, was dem-
onstrated in studies of house mice by Brown (1953), Christian (1955a, 1955b), Southwick (1955a,
1955b), and Strecker and Emlen (1953). Further examples of confinement effects in house mouse
populations were provided by Calhoun (1973) and Lidicker (1976). Calhoun (1962a, 1962b, 1963)
described similar patterns in Norway rats. The pathological nature of many of these effects was
pointed out by Anderson (1961) and Calhoun (1962a, 1962b). Parallel results were obtained with
confined vole populations at an early date (Clarke, 1955; Louch, 1956; van Wijngaarden, 1960).
94 Rodent Dispersal
Attribution of the discovery of such so-called “fence effects” to Krebs et al. (1969) by MacArthur
(1972), Tamarin (1978), and others seems inappropriate in view of the numerous earlier obser-
vations. What is important here, however, is the existence and nature of the confinement syndrome
and its relevance to the RFH and EFH.
The common characteristics of the syndrome, as seen in the references cited above, may
include violent fighting leading to wounding and death among sexually active males, loss of
weight and condition in subordinate individuals, multiple (and frequently sterile) copulations,
infanticide, persecution of juveniles (males in particular) at the onset of sexual maturity, and
inhibited sexual maturity or suppressed reproduction of young of one or both sexes. The pattern
develops more quickly when unrelated individuals are confined together than when a population
is initiated with a single pair (Brown, 1953), implying that the phenomena are not associated
with inbreeding. Adrenal hypertrophy, indicative of physiological stress responses among sub-
ordinate (potentially emigrant) individuals, has been evident where tests were conducted (e.g.,
Christian, 1955a, 1955b, 1956). Male offspring are usually the first to be affected and mortality
of male offspring is typically higher than that of females (Singleton, 1985).
Several points stand out in the present context. The first is that young are consistently the first
and most severely affected by the confinement syndrome. Two interpretations are possible. The
first is that all young are innate emigrants and frustration of their innate impulses generates the
pathologies. The second is that the syndrome is the result of pressure exerted by established
adults and that both adults and young suffer from the effects of behaviors that fail to produce
normal consequences. The evidence is strongly in favor of the second explanation. As predicted
by the RFH the young are objects of adult persecution, particularly at the onset of puberty, and
established adults (commonly the original founders of the confined populations) are the last
affected and show the least response, although they do eventually show stress symptoms and
abnormal behaviors. In extreme cases infants are killed, but more often young of both sexes fail
to reproduce. Female young, in particular, may fail to mature, and any young males that pass
through puberty suffer from attacks by breeding adult males. In view of the evidence that young
are philopatric given the opportunity to settle on the natal site, and the observation that young
are persecuted by resident adults, the RFH is strongly supported.
Seen in experimental enclosures, the confinement syndrome reduces the fitness of both residents
and their offspring, and may eventually lead to extinction of the confined population (e.g.,
Calhoun, 1973). Rodent populations inhabiting small islands are also confined, although, as shown
by Pokki (1981), the surrounding water barriers might be crossed more easily than cage walls.
Also, drowning of emigrants may provide a built-in system for disposing of “excess” individuals.
The peculiarities of populations of rodents on small islands, reviewed in detail by Gliwicz (1980),
reflect the confinement syndrome and/or its evolutionary aftermath.
On very small islands the probability that colonizing populations will succumb to the con-
finement syndrome may be high. In those populations that survive a confinement syndrome
phase and persist for many generations, stringent selection may have acted in several ways to
reduce or eliminate the confinement syndrome. The nature of any compensatory adjustment is
relevant to evaluation of the RFH. Observed “adjustments” include reduced aggressiveness of
adults (Halpin, 1981; Halpin and Sullivan, 1978; Tamarin, 1977a, 1978), and delayed or inhibited
maturity of offspring (Bujalska, 1970, 1971, 1973). Other characteristics of island populations,
listed by Gliwicz (1980), include: high and stable densities; low reproductive rates; low disap-
pearance rates of weaned individuals; density dependent mortality of nestlings; small, closely
packed home ranges; and control of recruitment by inhibition of female reproductive activity.
The association of demographic stability with lack of emigration sinks, proposed by Tamarin
(1977b), might actually reflect the general syndrome of resident adaptation to long-term island
existence. Island populations that do not display some of these adjustments, and show patterns
resembling those of experimentally confined populations (e.g., Adler and Tamarin, 1984), could
be of relatively recent origin.
Testing RFH 95
Summary
Although there are many gaps in our information, there is considerable support for the RFH.
Site tenacity is well developed, if not universal, among breeding adult rodents. Young are strongly
philopatric, settling on their natal sites if permitted to do so. Both adults and young have the
ability to discriminate among conspecifics as to sex, sexual status, degree of familiarity, relatedness,
and social status. Residents are aggressive toward strangers, and immigrants are more likely to
settle if residents are removed than if they are present. There is evidence for considerable
inbreeding, and it is questionable whether the costs of inbreeding outweigh the costs of avoiding
it. Selection for incest avoidance is compatible with either EFH or RFH; instances of incest
avoidance are open to alternative explanations and incest avoidance alone appears inadequate
as an explanation of emigration patterns. Evidence is abundant that male interactions are strongly
influenced by competition for copulations, and female interactions are similarly influenced by
availability of resources required for gestation and lactation. The resulting patterns of behavior
are in conformity with the assumptions of the RFH. Mothers are nepotistic, but more so toward
daughters than toward sons. Fathers have less assurance of relatedness, interact much less with
offspring, and are generally neutral toward prepubertal young. Delayed sexual maturity of young
could serve parents as a means of suppressing competition and conserving young at the natal
site, and serve young of either sex as a means of avoiding pressure to emigrate. The evidence is
largely circumstantial on this, as it is on such topics as mate preference, the actual stimuli for
emigration, the responses of potential emigrants to such stimuli, the behavior of transients, and
the process of immigration. Although many of the relevant questions remain to be investigated
in these areas, the trend of the evidence is compatible with the RFH. Strong support for the
RFH is evident in the confinement syndromes exhibited by experimental and island populations.
V
COMPARING THE RFH AND EFH:
PREDICTIONS AND TESTS
To what extent do the behavioral, demographic, and genetic patterns implicit in the RFH
differ from those of the EFH? To what extent do they provide a basis for tests that could assist
in evaluation of the relative applicability of the two hypotheses? In this chapter I have expanded
on some predictions, suggested others, and commented on specific approaches that could be of
use in testing the relative applicability and significance of RFH and EFH, in explaining the
evolution of dispersal among rodents, and in predicting the consequences of dispersal-related
behaviors.
Despite the risk of too much preaching, I think it necessary to remind readers of some basic
points. If these hypotheses are to be tested, both the concepts under investigation and units used
must be unambiguously defined. Emigration must be separated from immigration. Significant
stages in ontogeny must be clearly discriminated. Potential emigrant cohorts must be precisely
identified and those individuals that emigrate must be compared with those that do not if an
investigator wishes to test an hypothesis about the qualities of emigrants. Despite the great
difficulty involved, more ingenious and precise ways must be devised to discriminate potential
emigrants (including both established residents and unestablished individuals), actual emigrants,
transients, and immigrants. It is not appropriate to identify immigrants and transients captured
on a removal plot as emigrants. It is particularly inappropriate to regard such a sample as
representative of emigrants from an arbitrarily designated area nearby without precise knowledge
of the spatial origins of animals in the sample.
Testing the RFH demands that season be taken into account in all analyses of dispersal. Because
the RFH predicts seasonal variation in parental tactics and offspring responses, the practice of
pooling data on emigration, or emigrant characteristics, for an entire year, or an entire breeding
season, cannot be expected to give unambiguous results. In fact, one way of discriminating
between EFH and RFH explanations of emigration is through experimental manipulation of
parental (established resident) pressure, appropriately timed to test specific RFH predictions.
The RFH rests on several fundamental propositions reiterated here because it is essential that
the foundations of the hypothesis be kept clearly in view. They are: 1) that breeding rodents
establish fixed home ranges; 2) that emigration of young is caused by the behavior of residents
toward non-residents (in particular their own offspring); 3) that behavior of parents toward
offspring can change between treatment of young as the output of parental reproductive in-
vestment and treatment of young as competing, although related, conspecifics; 4) that young
endeavor to settle at the natal site and will do so unless forced to move elsewhere; and 5) that
residents effectively resist immigration.
Lidicker (1985b) criticized a preliminary version of the RFH (Anderson, 1980) on the following
grounds: 1) that it failed to account for observations claiming to have demonstrated a high
proportion of adults, especially adult females, among emigrants; 2) that it negated selection as
a result of advantage to emigrants; and 3) that the model did not predict that littermates will
depart synchronously. As discussed above, I believe that most reports of adult emigration are
based on inadequate definitions of adult and/or emigrant status. Littermates would be at least
as likely to depart synchronously under the RFH as they would if alleles for the tendency to
emigrate were segregating, and Lidicker (1985b) was incorrect in stating that the RFH does not
predict simultaneous departure of littermates. He is correct, of course, in stating that the RFH
96
Comparisons of RFH and EFH 97
assumes that emigrants are less fit than they would have been had they succeeded in settling at
the natal site, and I have summarized evidence indicating that this is the case. Comparisons of
the relative success of philopatric and emigrant young (e.g., Jones, 1986) are highly appropriate
tests of the two hypotheses.
Behavioral Predictions and Tests
The basic prediction of the RFH is that emigrants depart “because of” rather than “in order
to.” Emigration “in order to find a mate” (King, 1983) or “in order to find available space”
(Viitala and Hoffmeyer, 1985) is not anticipated. Emigrants are not expected to leave sponta-
neously due to “ontogenetic switches.’ Behavioral stimuli given by residents are expected to
precede emigratory responses on the part of offspring. To the extent that residents resist im-
migration, the movements of individuals unable to settle on, or adjacent to, the natal range are
likely to be prolonged and cover relatively long distances. Because the probability that travel
away from the natal site will be detected declines exponentially with distance, and the probability
of immigration might do so as well (see below), long-distance dispersal is considerably less likely
to be detected than short-distance dispersal. Recorded movements are probably even less rep-
resentative of distances over which an individual wanders before becoming established (or dying).
Despite this difficulty, it would help in comparing the two hypotheses if both dispersal distances
and transient movements could be studied more thoroughly and accurately.
The EFH and RFH make different predictions regarding dispersal distances. The RFH an-
ticipates that an emigrant should settle as close to the natal site as possible, benefiting by association
with relatives and minimizing risks of movement. Under this hypothesis, data on dispersal
distances should vary with season, density, and habitat distribution. Within a single cohort and
sex, leptokurtosis should be strong. In contrast, an extension of the genetic polymorphism hy-
pothesis might predict that the distance an individual moved (as well as the tendency to emigrate)
would be predetermined, and that dispersal distances might be bimodal or approximate a normal
distribution.
Historically, it was the observation that distributions of dispersal distances were leptokurtic
that inspired the EFH view that emigration was controlled by the genotype of potential emigrants.
Variation in emigratory drive seemed the simplest explanation for this distribution. The superficial
application of Occam’s law may not, however, provide the best answer in this case. Waser (1985)
demonstrated that a model assuming parent-offspring competition and offspring expulsion also
predicts a distribution of dispersal distances with a shape that closely approximates the leptokurtic
distribution observed for Peromyscus maniculatus by Dice and Howard (1951), yet does not
require any polymorphism in dispersal tendencies. The data did show two deviations from the
predictions of the Waser model: females tended to settle closer to the natal site than expected,
and there was an excess of long distance movements. Neither phenomenon has been explained
on an emigrant-fitness basis.
The RFH offers explanations for the philopatry and short dispersal distances of female young.
It may also suggest some explanations for an excess of long distance movements. As an individual
moves farther away from the natal site there will be a decline in the mean relatedness of residents.
If individuals are more tolerant of relatives than non-relatives, and if mate choices favor slightly
different phenotypes and discriminate against greater differences, the probability of social ac-
ceptance might drop off rapidly with dispersal distance. Once a transient has passed an inter-
mediate zone the probability of immigration may be low, and wandering may be prolonged. It
may also be that a transient would be influenced by the similarity or dissimilarity of the habitat
to that at the natal site. As distance from that site increased, acceptability of the habitat might
decrease. These effects could account for long-distance movements. Both the relatedness effect
and the habitat effect should be testable.
How far might a transient travel from the natal site? Small rodents clearly have the capability
for rapid long-distance movement (Beer, 1955; de Kock and Robinson, 1966; Getz et al., 1978).
Sadykov et al. (1985) recorded movements of radioisotope-marked transient Clethrionomys as
98 Rodent Dispersal
1,500 m in 24 h. An individual traveling at this rate along a canalizing habitat such as a stream
course might cover 10 km in a week. Transients traveling for more than a few hours clearly are
capable of moving beyond the limits at which they can be detected in most studies. They almost
certainly do precisely that. Hilborn and Krebs (1976) radioactively-tagged 219 Microtus town-
sendii in an attempt to identify and follow emigrants. Only 30 tags were recovered, and Hilborn
and Krebs felt that most explanations other than long-distance movement could be ruled out. If
rates of movement evident in the study of Sadykov et al. (1985) and implied by the results of
Hilborn and Krebs (1976) are typical, then studies of emigration using small grids (or within
enclosures) would give misleading results.
The RFH predicts that long-distance movements should be made primarily by males and
should be most frequent when competition for mates is high (e.g., in the spring), both of which
were observed by Smyth (1968) for Clethrionomys glareolus and by Crawley (1969) for C.
glareolus and Apodemus sylvaticus. Females born early in the breeding season should move
only short distances. Female dispersal distances should increase for later cohorts. Long-distance
dispersal by females would be promoted if females can mate prior to emigration or while transient.
A clear-cut, but difficult-to-test, difference between the RFH and EFH may exist in the
relationship between fitness and dispersal distance. This is illustrated in Fig. 1. The EFH predicts
that fitness of offspring should increase with distance from the natal site until any advantages
of movement are overridden by the costs of reduced survival and/or delayed reproduction,
thereby producing a simple convex frequency distribution. In contrast, the RFH predicts that
the general trend is for fitness to decline with distance moved. For female offspring this decline
should begin at the spatial limit of maternal nepotism. Beyond that zone, further decline in
fitness would be a result of time lost in relation to the limited female potential to produce
offspring. For males, faced with paternal competition and unassisted by nepotism, a much lower
initial fitness and a more drawn-out distribution (reflecting the potential of a polygynous male
to mate repeatedly with several females) is suggested.
The timing of emigration might also be useful for discriminating between the EFH and RFH.
The RFH predicts that emigration should occur primarily within the breeding season. With the
exception of some terrestrial sciurids this prediction is borne out (e.g., Krohne et al., 1984;
Myllymaki, 1977a; Smyth, 1968). Patterns such as the burst of emigration of overwintered
Peromyscus coincident with the initiation of breeding, and leading to colonization of sites made
vacant by winter-induced mortality, are consistent with RFH predictions. If breeding is exper-
imentally prolonged (e.g., by supplemental food) emigration should be prolonged as well.
As Horn (1983) suggested, a parent should behave so as to maximize the chance that its
offspring will outcompete the offspring of other parents for occupancy of the natal site. It also
follows from the RFH, and from models by Hamilton and May (1977) and Comins et al. (1980),
that parents should suppress emigration of offspring whenever there is a period of parental
reproductive quiescence in which the probability of parental survival is lower (less than half?)
than that of philopatric offspring.
In seasonally polyestrous species emigration commonly ceases with cessation of breeding as
the RFH anticipates it should, but emigration has sometimes been reported to be high in the
immediate postbreeding period. Many such reports, however, deal with the number of transients,
rather than the proportion of potential emigrants that actually move. Where this is the case the
trend isa reflection of high post-breeding numbers, rather than of high emigration rate. Movement
outside of the breeding season, on the basis of the RFH, should be more or less random with
respect to sex and age. Singleton (1985), using both “exit’’ and “entrance’’ traps in mouseproof
fences surrounding haystacks, reported that in non-breeding populations, house mice leaving
and re-entering the fenced areas did not differ in sex, age, or mean weight from those that
departed permanently.
The EFH and RFH offer different explanations for male bias among emigrants. There has
been no specific elaboration of “innate” and “pre-saturation”’ versions of the EFH in this area,
but Greenwood (1980, 1983) has argued that male bias can be best explained on the basis of
selection for behavior (by parents or offspring) that restricts inbreeding. An EFH explanation
Comparisons of RFH and EFH 99
EFH
ALENESS ==
oe
a
DISTANCE ——>
RFH
FITNESS ——>
Oy
+O
DISTANCE ——>
Fic. 1.—Qualitative patterns in the distribution of fitness relative to distance moved during dispersal as
predicted by the Emigrant Fitness (EFH) and Resident Fitness (RFH) hypotheses.
based on selection for behavior of male offspring might require that alleles programming emi-
gratory tendency be sex-linked, or sex-limited in expression. The RFH requires neither. It predicts
that: 1) emigration will be closely associated with puberty in both sexes; 2) males will be more
likely to emigrate than females because male parents tend to expel all male offspring as long as
paternal residual reproductive value is high; 3) females tend to expel some males; 4) males do
not expel females; and 5) females expel only a few females.
Fisher (1958) and many subsequent theoreticians have examined the question of sex ratio at
100 Rodent Dispersal
birth and generally have concluded that equal numbers of males and females should be produced.
Although I do not feel competent to undertake a mathematical approach to the topic, I suspect
that the same arguments could be applied to the “return” (transmission of parental alleles to
future generations) that parents receive through disbursement of their offspring. If this is correct,
the RFH predicts that parents should disburse male and female offspring in such a way that the
production of grandoffspring through sons and daughters is equal. This should be reflected in
comparisons of the sex ratios among emigrants and immigrants, and the relative reproductive
success of the sexes following immigration.
Trivers and Willard (1973) postulated that if males competed for copulations and if large
body size were advantagous, then male offspring would be selected for rapid growth and large
body size. Where that was true, mothers might benefit by varying the sex ratio of young on the
basis of their own available resources. If return is proportionate to parental investment, females
in poor condition should produce the less expensive sex, whereas those in good condition should
produce the more expensive sex. Trivers and Willard reviewed data that appeared to conform
to this hypothesis. This line of reasoning seems applicable to parental strategies with respect to
the export of offspring. The point is that if parents behave so as to maximize return on their
investment, Fisher’s (1958) argument should apply here as well—in other words, the return on
disbursement of male and female offspring should be equivalent. In rodents there may be little
difference in maternal investment in males and females if there is little dimorphism in body
size, but sexual dimorphism in size has not been thoroughly investigated. If the cost of producing
sons and daughters is the same, but male offspring have the potential to transfer parental alleles
through multiple matings and females have a much lower potential, female offspring should be
conserved through nepotism. It also follows that male bias in emigration should be greater in
polygynous species.
How should resident strategies vary with population density? The RFH anticipates that resident
behaviors toward offspring will be relatively insensitive to crude density. Male behavior, in
particular, should show little variation with density. There is little reason for a male to be more
aggressive toward sons at high density than at low density. Similarly, although resident females
may be less able to abdicate in favor of their daughters and find a nearby range for themselves
if all nearby areas are already occupied, full occupancy of available space need not affect the
general level of resident female aggressiveness even though females may be forced to expel sons
or daughters. In unconfined populations it is not necessary, with respect to either male or female
residents, to assume with Krebs (1978b) that as density increases there is no alternative to fighting
to maintain fitness. Immigration could still be prevented if transients avoid contacts with residents,
perhaps by responding to resident scent marks. Emigration of offspring might still be stimulated
by parental behavior that is relatively benign. There have been few studies of interactions between
resident parents and their offspring in natural contexts, and most of the evidence for parental
expulsion of offspring is circumstantial rather than direct.
Still another potentially useful distinction between RFH and EFH exists with respect to the
nature of emigratory stimuli. The RFH predicts that the stimuli will be external, but that because
parents gain fitness by optimizing the emigration of their offspring, emigrants that are forced
to leave should not be damaged. Because fathers can benefit by altruism toward sons, resident
males should expel presumed sons without harming them. Paternally administered wounding of
young males should occur only when normal processes are obstructed. In confined populations
that were regulated by removals, Hestbeck (1986) found that Microtus californicus identified
as emigrants had a lower incidence of wounds than they did in confined populations not so
regulated. Wounding, on the basis of Hestbeck’s results, appeared to be a pathology induced by
confinement, a result which would be predicted by the RFH but is not inherent in the EFH.
Authors have varied in their thinking as to how potential emigrants should respond to increases
in density. Stenseth (1983) suggested that philopatry would be high following a decline in density
and restriction of voles to the most favorable habitat patches, and that as density increased,
individuals with a tendency to emigrate would be favored. Emphasizing the heterogeneity of
Comparisons of RFH and EFH 101
microtine habitat, Lidicker (1985b) suggested that when regional (metapopulation) density was
low, small demes with high probabilities of extinction occupied the superior microhabitats, while
surrounding and inferior habitats served as “sinks.” He envisioned that the probability of an
individual’s emigration from such a population would be high, and that as density increased,
emigration would decline because potential emigrants would be prevented from leaving the
natal site by the resistance of surrounding residents (the “social fence’ hypothesis of Hestbeck,
1982, 1986). Hestbeck (1986) demonstrated inhibition of emigration with increasing density in
a confined population, but it remains to be seen if this would occur in less artifical situations
(other than on small islands).
Whether increasing density lowers the emigration rate as visualized in the social fence model
depends in part on the interaction between residents and transients. If residents are required to
eject transients forcibly, as would be expected on the basis of arena experiments, young might
be forced back to the natal area as Hestbeck (1982) and Lidicker (1985b) have envisaged. If
transients are not attacked, and are allowed free passage as is indicated by the more tolerant
behavior of resident M. pennsylvanicus toward strangers than toward unrelated neighbors re-
ported by Skirrow (1969), emigration may not be inhibited by density. Lidicker’s model appears
realistic with respect to dispersion, but somewhat contradictory with respect to emigration rate
because it envisages that panmixia will increase in conjunction with inhibition of emigration
(Lidicker, 1985b). It also appears inconsistent with the EFH because emigrants lose fitness
whatever the density. They are expected to be largely absorbed by “sinks” when regional density
is low, and to be prevented from departing when it is high.
The RFH predicts that philopatric tendency in offspring is essentially constant and therefore
insensitive to crude density. This, together with the strategies attributed to residents, should
minimize density-dependent variation in the probability that young will emigrate. To the extent
that the literature reflects the probability of emigration, this seems to be the case (e.g., see the
conclusions of Gaines and McClenaghan, 1980).
Several experimental removal approaches can be envisaged that would be useful in discrim-
inating between EFH and RFH with respect to the relationship between emigration and density.
Specifically, the techniques used by Redfield et al. (1978a, 1978b) and Boonstra and Rodd (1983)
could be modified and extended through still more selective removals of specific sex-age cohorts.
In one pertinent experiment producing results consistent with RFH prediction, Rodd and Boonstra
(1984) found that reduction in the density of overwintering M. pennsylvanicus improved per-
sistence rates of males in the spring, but did not affect persistence of females.
As suggested earlier, the RFH predicts that within a breeding unit, removal of a resident of
one sex during the breeding season should favor philopatric recruitment of an offspring of that
sex. Immigration should be similarly favored. Removing residents is the simplest way of varying
pressure on young, but mass removals (“removal grids’’) are bulldozer approaches where surgical
precision is needed. I suggest that removal of single resident individuals of one sex or the other
from numerous well-separated sites, and monitoring of the fates of potential emigrants (young
born on the home ranges of the adults removed, or on adjacent home ranges), should replace
mass removal approaches in testing the validity of hypotheses about resident pressure and its
effects.
According to the RFH an isolated pair would still export their young according to the strategies
outlined in Chapter II. Removal of a male should increase the probability that a son of that male
would settle. That probability should be independent of density. Single pairs could be studied
in large enclosures or through introductions to islands in order to test this prediction. If it proves
correct, alternative and simpler explanations of the observations that have led to the concepts
of “‘pre-saturation” and “innate” departure of young would be available. Removal of maternal
females should prevent or reduce emigration of male young in seasonally monestrous species
such as Spermophilus beldingi.
The work of Stoddart and others (e.g., Stoddart et al., 1975) on the role of scent suggests many
possible experiments through which the role of odor in facilitating nepotism and philopatry and
102 Rodent Dispersal
in controlling emigration and immigration can be investigated. The RFH predicts that in pop-
ulations in which males make little post-copulatory investment in their young, and male-male
competition is centered on copulations, emigration of young males should be delayed if female
scent is applied to them. Less directly, emigration of young males should be inhibited by removal
or neutralization (e.g., castration, hormonal manipulation, olfactory blocks) of fathers or by any
measures that delay or prevent maturity of young males.
Holekamp et al. (1984) suggested that emigration might be a direct response to the level of
gonadal steroids in male Belding’s ground squirrels, arguing that if emigration had evolved as
a means of avoiding inbreeding, a direct physiological (EFH) mechanism effecting male emi-
gration independent of environmental conditions might be adaptive. Where this EFH hypothesis
predicts an inflexible response, the RFH predicts that increasing steroid levels in potential
emigrants would fail to induce emigration in the absence of resident pressure. Taitt and Krebs
(1982) reported that residency times of female Microtus implanted with testosterone were lower
than those of control females, and equivalent to those of males. Disappearance due to death and
disappearance due to emigration could not be distinguished, however. The Holekamp hypothesis
could be tested by removing male residents while artificially raising androgen levels in their
male offspring.
Manipulation of food and cover might also produce informative data if carried out in con-
junction with selective removals. The RFH predicts that as long as there is no acute shortage of
food or cover, removal of resident males should facilitate philopatry of male offspring exclusively,
whereas removal of resident females should encourage philopatry in females. When material
resources are short, on the other hand, removal of males might have no effect on philopatry of
male offspring because females should then expel male offspring to reserve resources for them-
selves and their daughters. Food supplementation at a time of resource shortage should encourage
female recruitment, but have a less marked effect on male recruitment or male emigration.
Application of male scent to female young (olfactory masculinization) should cause their emi-
gration irrespective of resource levels. These predictions are not derivable from the concept of
an innate tendency to emigrate that is implicit or explicit in most interpretations of the EFH.
Tests of behavior could also be devised in the area of cohesiveness and mate selection. It will
be important to determine if the barriers to inbreeding adduced on the basis of laboratory studies
function in nature; the RFH predicts that they would not be significant, whereas the EFH
emphasizes avoidance of inbreeding. According to the EFH, for example, probability of successful
immigration might be inversely proportional to degree of relatedness. The RFH predicts that
probability of immigration should be positively correlated with relatedness. If inbreeding is
unimportant, removal of resident males should increase the probability of their sons establishing
at the natal site more than it should the probability of establishment of unrelated males.
Experiments designed to test both the incest avoidance hypothesis and various EFH and RFH
predictions could be carried out through systematically varied releases onto uninhabited islands
or into large outdoor enclosures. Comparison of the histories of populations initiated with sibling,
non-sibling, and cross-fostered pairs of colonists in such contexts should be informative. It would
also be of interest to know if there is any evidence of incest avoidance among ‘siblings’ belonging
to different litters, or among overwintered young. Inbreeding and outbreeding need to be
evaluated on the basis of cost versus benefit rather than cost only. Avoidance of inbreeding
appears to be one of the stronger and more popular supports of the EFH. Costs of inbreeding
are clearly a legitimate point on which to question the RFH, but potential benefits of inbreeding
strengthen the RFH.
Because the RFH postulates normal distributions of emigratory tendency among potential
emigrants, a variety of direct tests of emigratory behavior might be useful. The individuals to
be compared come from the same source population and belong to the same seasonal cohort of
young, and tests could be extended to comparison of breeding colonies derived from parents
that were assumed to differ in emigratory tendencies. If some criterion were chosen to discriminate
between supposed “‘pre-saturation” and “saturation” phenotypes, for example, colonies derived
Comparisons of RFH and EFH 103
from each should be developed. The RFH would predict that comparable cohorts from the two
colonies would not differ in behavior under identical test conditions, indicating that the presumed
difference was not inherent, but due to external influences. If there is variation in tendency to
emigrate, it might be discernible as differences in individual responses among members of the
same sex-age cohort to experimental displacement just beyond the limits of the maternal home
range.
The greatest void in the study of dispersal is in the areas of recruitment and immigration. As
a starting point, the assumption that young are inherently philopatric should be tested thoroughly.
The simplest approach is to mark individual litters and explore the effect of removing one or
both parents. The generality of the observation that young that do not succeed in obtaining
rights to the natal site and settle instead in the first vacancy in suitable habitat, as observed by
Baird and Birney (1982b), should be determined.
According to the RFH, females should have higher average success in immigrating than males,
and males that emigrate should remain transient longer, wander more widely, and suffer higher
mortality following emigration than females. Each of these predictions can be tested by exper-
imental displacements. Female-scented or sexually inactive males should be more successful in
establishing residence than sexually active males. Male-scented females should have reduced
success. Immigration should be sensitive to manipulation of resident female behavior. As Taitt
and Krebs (1982) observed, masculinization of resident females, like removal of females, should
result in increased immigration of both sexes. As the RFH would predict, treatment of resident
females with the chemosterilant mestranol apparently reduced their ability to maintain resident
status (the cause of their disappearance was unknown).
Young of both sexes should benefit by philopatry and by association with kin. Few tests have
been made, but Jones (1986) was able to demonstrate that philopatric young Dipodomys spec-
tabilis benefited by maternal abandonment of the natal mound. He was, however, unable to
find evidence that proximity to kin increased survival. Further tests of this type would be useful.
Habitat selection studies also have a place. Male transients should attempt to select habitat on
the basis of female availability. Female transients should select sites on the basis of resources
required for rearing young. Getz et al. (1987) have predicted that in Microtus ochrogaster new
breeding units form when unfamiliar males and females meet in neutral areas.
Short-distance displacements would serve as a test for residency (i.e., individuals that home
can be defined as residents, those that do not can be defined as unestablished). At the release
site the unestablished individuals are potential immigrants. The RFH predicts that the probability
of displaced non-residents immigrating should vary with the relatedness of the residents within
whose home range they are released. The effects of season, and of the ontogenetic stage of
displaced individuals, would also be of interest when displacement techniques are used.
Demographic Predictions and Tests
If the RFH is to be tested in a demographic context, several precautions need to be kept in
mind. The first is that care should be taken to distinguish between the measurements of the
number of emigrants or transients and the proportion of emigrants or transients. As Stenseth
(1983) pointed out, this distinction has sometimes been overlooked. The second is that the
measurement of emigration rates as the proportion of actual emigrants to potential emigrants
should be specific to carefully chosen and defined sex-age cohorts at each season. As shown by
Beacham (1980), attempts to correlate emigration rates with demographic trends have often
mistakenly interpreted seasonal trends in emigration rate as reflecting “cyclic phases’ in de-
mography. Many authors, when relating density to emigration rates, have failed to distinguish
between long-term trends (‘‘phases” of population demography) and trends that were part of
the annual cycle. On careful examination, the “increase phase” in the majority of purported
correlations between emigration rates and supra-annual or multiannual density trends turns out
to be synonymous with at least the latter part of the annual reproductive cycle when, as the
RFH predicts, populations are open to recruitment of young. Krebs et al. (1973) have argued
104 Rodent Dispersal
that because it frequently appears that emigration in microtines is maximal prior to a population
decline, the relationship between population density and emigration must be qualitative rather
than quantitative. The RFH correctly predicts the temporal relationship to which Krebs et al.
referred. In doing so it provides an alternative explanation through analysis of possible strategies
of residents and seasonal cohorts of young. It thus accounts for a relationship between emigration
and crude density, which in most, if not all, of the published examples is directly associated with
the cycle of seasonal reproduction.
Some data (e.g., Mazurkiewicz and Rajska, 1975) show declining emigration with increasing
density. The social fence hypothesis (Hestbeck, 1982) offers one explanation, assuming that
resistance to transient movement increases as density increases and that the advantage to dominant
individuals in expelling a subordinate should decrease as density increases. Mares et al. (1982)
carried out experiments designed to discriminate between the effects of resource availability and
density per se on movement patterns in chipmunk populations and concluded that movement
was not directly affected by density. The RFH predicts declining emigration as density reaches
its seasonal peak, but makes this prediction on an entirely different basis (the advantage to
residents of conserving their offspring as their own residual reproductive value declines). I suggest
that the demographic observations that the social fence idea was proposed to explain are largely
season-based, rather than density-based, and that when season is taken into account the patterns
in emigration rate will be explicable without the need of an additional hypothesis.
The RFH implies that although emigration is not strongly density dependent, immigration
well may be. It is not inevitable, however, that transient movement, as distinct from immigration,
is restricted by increasing density. Tests of density effects should be devised so that it is possible
to discriminate between immigration and transient passage. Multivariate analysis of disappear-
ance rates by Gaines and Johnson (1984) pointed to season as the most important variable in
explaining the ratio of presumed transients to residents in heavier (older) Microtus ochrogaster.
For lighter (younger?) individuals season was not as effective for explaining variation in this
ratio. This is contrary to RFH expectations. Re-examination of this result and those of other
studies would be valuable in order to determine if a large proportion of the unexplained variation
may have resulted from difficulties in categorization.
In addition to more precise and relevant categorization, improvement in demographic measures
would be helpful. The “replacement rate” or “recovery ratio,’ defined as total catch on a removal
plot divided by the catch on a neighboring control plot (e.g., Fairbairn, 1978a), is an inadequate
and probably misleading measure of emigration. It identifies neither the cohort(s) nor the origin(s)
of individuals in the sample that the removal plots have drawn from the transient pool; there is
little justification for the assumption that it monitors the emigration rate on a nearby “control”
plot. If replacement is to be measured, a better approach might be to measure it directly through
selective removal of individuals rather than mass removals.
According to the RFH, the emigration rate should be independent of density over a wide
range. To the extent that the techniques used to date actually reflect emigration, emigration
rates do not appear to be density dependent (Gaines and Johnson, 1984; Gaines and McClenaghan,
1980; Verner and Getz, 1985). Further experimental manipulation of sex ratios along the lines
exemplified by the studies of Krebs et al. (1978) and Boonstra and Rodd (1983) should be
designed to test RFH predictions as to demographic effects at different seasons.
Boutin et al. (1985) reviewed four hypotheses that have been proposed with respect to the
relationship between the emigration rate and the trend in crude density. These were termed the
pre-saturation/saturation hypothesis, the kin-selection hypothesis, the selective dispersal hypoth-
esis, and the food shortage hypothesis. In their view, predictions for emigration rate and growth
had not been stated explicitly for the pre-saturation/saturation hypothesis, but as interpreted by
Stenseth (1983) the emigration rate should be expected to increase with increasing density.
According to the kin-selection hypothesis (Charnov and Finerty, 1980, as expanded by Stenseth,
1983), an increase in density would bring about a decrease in the mean relatedness of interacting
individuals, leading to higher levels of aggression, and thereby stimulating higher rates of em-
Comparisons of RFH and EFH 105
igration. The selective dispersal (emigration) hypothesis postulates that emigration-prone phe-
notypes predominate in increasing populations. The food shortage hypothesis reduces simply to
the expectation that hungry animals will move in search of food. Each of these models appears
to me to be too coarse to provide results that are other than superficially plausible or misleading.
The analysis of Boutin et al. (1985) illustrates the point that the predictions of the pre-saturation /
saturation hypothesis are so vague as to be open to contradictory interpretations. The pre-
saturation/saturation and kin-selection hypotheses rely on assumptions regarding the nature and
frequency of social interactions that have never been demonstrated in nature, and for which
there is contrary evidence. For example, Mazurkiewicz (1981) found that although home range
size in Clethrionomys glareolus decreased with increasing density, the number of voles per trap
station did not increase. The observations of Pearson (1960) also point to the conclusion that
social pressure is not simply or directly related to density. The selective dispersal hypothesis
likewise postulates undemonstrated phenomena: the existence of innate trends in density, and
the existence of phenotypes that detect and make specific responses to such trends.
Although the demographic predictions of the EFH, at least as enunciated to date, are ex-
ceedingly vague, those of the RFH are relatively specific and more readily testable. The RFH
predicts that although crude density should have relatively little influence on the probability
that young will be expelled, density would influence the distance traveled by transients, and the
probability of their establishment at a new location. Tests designed to discriminate between the
two hypotheses on the basis of density responses should concentrate on family units. The RFH
predicts that per capita probability of emigration from a matriline, or other family unit, will be
sex, age, and season specific, but largely density independent. Male emigration is expected to
increase in seasonal breeders during the pre-reproductive period (in association with male com-
petition and the commonly observed pre-reproductive population decline). Throughout the
mating period the probability that young males undergoing puberty will emigrate is predicted
to be high whether the population is increasing or decreasing. Female young undergoing puberty
will have a high per capita probability of emigrating whenever resident breeding females are
stressed by food shortage. Per capita probability of emigration of young of both sexes is predicted
to decline in polyestrous seasonal breeders during the period of maximum recruitment at the
end of the breeding season.
If there are any density dependent effects on the probability that an individual will emigrate,
the RFH predicts that they will be related primarily to resident female density. Female emigration
rates are predicted to correlate positively with shortages of food, or unavailability of space. Male
emigration will be unlikely to show cause and effect relationships with density. At times when
emigration of male young is dependent on paternal pressure, experimental removal of male
offspring should have little effect on the probability that remaining male siblings would establish
themselves at the natal site, but removal of young females should increase the probability of
philopatry for remaining female siblings. Removal of resident males should have no effect on
philopatry of female young. As long as resident males are in breeding condition, removal of
young females should fail to reduce the probability that their male siblings will emigrate (assuming
that food resources are sufficiently abundant to eliminate any resource-related effects).
The RFH can be used to generate specific, testable predictions for demographic histories.
Figure 2 presents a family of curves representing the relationships among resources, absolute
crude density, economic density (per capita resource availability), effective density (individually
perceived density including interference competition), emigration, and recruitment as these
might be predicted on the basis of the RFH in a microtine population. Contrasting patterns are
outlined for continuously occupied (core) and opportunistically or seasonally occupied (coloni-
zation) habitat. A projection as to the evolutionary contribution of animals breeding in the two
habitat types, also included in the figure, reflects the relative contribution of residents and
emigrants to the ongoing metapopulation inhabiting the surrounding region. The figure illustrates
both the specificity of RFH predictions and the many points at which tests could be designed.
In such an RFH model, the emigration rate tracks stochastic patterns of environmental quality
106 Rodent Dispersal
CORE COLONIZATION
HABITAT HABITAT
FOOD AND SPACE
EVOLUTIONARILY EFFECTIVE POPULATION
+ + i |
+ v |
+ + +
.
O
BREEDING BREEDING
SEASON SEASON
VW Emigration _A Immigration _/\ Recruitment
Fic. 2.—RFH-based predictions for a hypothetical vole population, specified for a stable patch of contin-
uously occupied (core) habitat and a patch of seasonally or occasionally suitable (colonization) habitat.
Comparisons of RFH and EFH 107
primarily through female assessment of resource availability and consequent emigration of
offspring. The predicted pattern of microtine abundance and emigration under “typical” con-
ditions, as shown in Fig. 2, and its possible modifications by variation in weather and resource
availability, should be compared with the results obtained in studies of Microtus californicus
by Bowen (1982) and Cockburn and Lidicker (1983), the 10-year data set provided for M.
pennsylvanicus by Mihok (1984), and other detailed descriptions of annual and multiannual
patterns in microtine demography.
To my knowledge no equivalent EFH predictions have been devised and published. In contrast
to specific predictions such as those outlined in Fig. 2, an EFH model would predict relatively
little difference between the probability that male and female young would emigrate, no dif-
ference in the timing of male and female emigration, a greater response to crude density, and
less specificity with respect to season. Alternatively, an EFH model might predict simply that
in the absence of habitat destruction or resource shortage a constant proportion of the potentially
emigrant cohort should emigrate, regardless of density. The distinctive basic postulate of the
RFH is that emigration rates should be primarily responsive to economic density as perceived
by breeding females, and to residual reproductive value of residents of both sexes.
A recent study by McShea and Madison (1986) reported that in spring the sex ratio of juvenile
Microtus pennsylvanicus recruited into the trappable population was strongly biased toward
females (61.5 to 67%). In fall the sex ratio among such recruits proved to be even, or biased
(70.5%) toward males. Relative weight of nestlings was higher in females in the spring and lower
in females in the fall. Nestling loss within litters was negatively correlated with weight, suggesting
that ratios could have been influenced by differential survival. Heavier (possibly overwintered)
females produced female-biased litters toward the end of the breeding season. This study implies
a facultative seasonal bias in investment in nestlings. Such shifting bias is in accord with the
RFH, which would predict that females should favor daughters as residual maternal reproductive
value declined.
There are other explanations for biased sex ratios. As Trivers and Willard (1973) proposed, a
female-biased sex ratio might reflect poor female condition and a consequent maternal disin-
vestment in male offspring, provided that the variance in male reproductive success is higher
than that of females and that when conditions are good investment in male offspring will lead
to their greater success in competition for copulations. Early season conditions may indeed be
poor. Fairbairn (1977b) noted that early-season breeding is costly to female Peromyscus. Lab-
oratory evidence supporting this theory has been provided by McClure (1981), who demonstrated
that food restriction led to a bias against males in neonatal growth and survival in Neotoma.
Trends in maternal pressure on male and female young to emigrate might reflect the interaction
of the same kinds of tactical responses.
In most transient-settler samples taken from removal plots, younger animals and males have
predominated (Gaines and McClenaghan, 1980). Absence of such biases in samples taken from
the transient pool (Joule and Cameron, 1975; Stafford and Stout, 1983) are open to several non-
exclusive explanations. As pointed out earlier, emigration is less likely to be governed by resident
behavior outside of the breeding season; such “template” results may be obtained when data
from an entire annual cycle are aggregated, obscuring seasonal patterns.
Comparison of results of pitfall and conventional trapping may be useful. From a study using
—_—
Resource availability, crude density, density in relation to the resources available (economic density) for
lactating females, and density in relation to social pressure and resources combined (effective density, graphed
separately for males and females during the breeding season) are shown as related to mean density on the
four upper graphs. The timing of emigration, immigration, and local recruitment are indicated by triangles
below the graph of effective density. The times at which male and female emigration are predicted to
predominate are indicated for core habitat. The lowest graph indicates the pattern of variation in relative
size of the group contribution to the subsequent regional gene pool.
108 Rodent Dispersal
pitfall traps, Kozakiewicz (1976) reported that peaks in the pitfall-vulnerable (“transient’’) com-
ponent of a population of Clethrionomys glareolus occurred in early fall in 1971, and in July
and August in 1972. At first glance this appears to be at variance with RFH predictions. However,
identification of the birth cohorts to which transients belonged showed that in both years they
came from the early and midseason cohorts, as the RFH predicts. Comparison of the results of
pitfall and live-trap registration of Microtus townsendii (Beacham and Krebs, 1980) showed
peaks in pitfall catches at times when the RFH would predict non-resident numbers to be
maximal. Trappability in live traps, in contrast, was highest in spring when breeding had been
established and the proportion of residents in the populations would be predicted to be at its
peak.
Most writers have assumed that the demographic consequence of emigration will be limitation
of density. Horn (1983) pointed out, however, that modeling studies are inconsistent. Some have
predicted density-increasing effects and others have predicted density-limiting effects. Emigra-
tion has also been supposed to be both a destabilizing (Tamarin, 1978) and a stabilizing (Anderson,
1970, 1980; Lidicker, 1962, 1975) factor in the dynamics of rodent populations. The RFH assumes
that populations are structured into small units, including local populations and matrilines, which
collectively make up a regional “metapopulation” along the lines envisaged by Anderson (1970),
Lidicker (1985b), and Stenseth (1983). It implies that the strategies of resident females will act
to promote stability in the small units occupying favorable habitat by regulating the retention
and reproduction of female offspring. Relaxation of intolerance by both sexes during the non-
breeding season may serve to stabilize density in the metapopulation by allowing more animals
to move into sites where the probability of survival is higher during the non-breeding months.
At other times, resident strategies may facilitate colonization of marginal habitats. When the
stochastic variations of the general environment make these marginal habitats unusually favorable
for long-term reproduction, emigration might be viewed as the causal factor in a consequent
population eruption.
Demographic predictions should, therefore, be viewed in the context of both predictable and
unpredictable changes in the environment. Mihok et al. (1985b) concluded that continual influx
of voles into a removal grid during midsummer tended to refute behavioral regulation of
population density. My conclusion is the opposite. Parental (primarily female) behaviors tend to
ensure a two-level population structuring in which semi-permanent breeding units export emi-
grants, maintaining a transient population available throughout the breeding season to fill gaps
created by experimental manipulations or environmental stochasticism. These same strategies
restrict increase in density and increase persistence of occupation in high quality habitats. The
RFH predicts that in the absence of confinement the primary effect of male aggressiveness is to
mediate emigration and immigration of males. Further, it implies that because male aggres-
siveness is probably constant over a wide range of densities, male aggression will have no density
dependent effect on the emigration rate.
In polygynous species, male aggressiveness should bias the operational sex ratio toward females
at all except the highest densities. Through export of sons and resistance to male immigration,
male aggressiveness should increase rather than decrease the reproductive rate and the per capita
rate of population growth. In general, male aggressiveness should limit population growth only
in situations where increasing density reduces either the opportunity for matings, or the returns
to males on post-copulatory reproductive investment. Further refinement of experiments in which
resident sex ratio is manipulated along the lines pioneered by Redfield et al. (1978a, 1978b) and
Boonstra and Rodd (1983) should be worthwhile.
It is probably not possible to overemphasize the often overlooked need to discriminate carefully
among seasonal cohorts of young in behavioral and demographic studies. The subadult stage
(encompassing both the puberty transition and the transition to resident status) is critical as each
cohort matures, and occurs in a distinctive context for each cohort. The RFH predicts differential
recruitment among seasonal cohorts. This is nicely demonstrated in simple form in the study of
Stoddart (1971), showing that Arvicola born into a discrete population before 1 July were
Comparisons of RFH and EFH 109
recruited, but those born thereafter were not. The distinctiveness of cohorts is relevant to the
Chitty-Krebs explanation of density fluctuation (Krebs, 1978a). One interpretation of the EFH
might predict that a constant proportion of each cohort would be emigration-prone (as suggested
by the data of Gaines and Johnson, 1984); another EFH interpretation might lead to the prediction
that this proportion would change as the result of selective forces driven by density responses,
particularly the aggressive responses of males. It is the second interpretation that is implicit in
the Chitty-Krebs hypothesis. The RFH contradicts both of the EFH models just described. Instead
of the simple Chitty-Krebs model of emigration driven by density-dependent selection, the RFH
proposes that variation in emigration rate is driven by a complex relationship among seasonally
variable habitat quality, resource availability as perceived by individual females occupying
habitats that vary spatially and temporally in their capacity to support survival and reproduction,
and male competition. Accordingly the RFH anticipates that interannual fluctuations should
show significant, and sometimes subtle, dependence on variation in annual weather patterns and
the phenology of food plants. The RFH model neither explains nor predicts intrinsic periodicities
in population density. A more careful examination of the question of whether microtine numbers
truly show regular multiannual periodicities than has been undertaken in the past (e.g., Elton,
1942; Finerty, 1976; Krebs and Myers, 1974) might eliminate the notion that such periodicities
exist, and thus obviate the need to explain them. The recent review by Taitt and Krebs (1985)
suggests that the concept of periodicity may indeed be on the way out.
Seasonal variations in the emigration rate may be useful criteria on which to judge the EFH
and RFH. In seasonal breeders the initiation of the non-breeding season is a time of maximum
recruitment and increase in density, coincident with onset of less favorable conditions such as
food scarcity or lower temperatures. As environmental conditions deteriorate, economic density
and competition should increase. The EFH postulates that individuals with a higher sensitivity
to competition (“pre-saturation emigrants’) should emigrate in response to increasing density
and/or deteriorating environmental conditions. On this basis, the EFH predicts that the emi-
gration rate would increase at this time. The RFH, in contrast, postulates that parents should
cease exporting young at the time when residual parental reproductive values are nearing
exhaustion, density is maximal, and opportunities for breeding are minimal.
Movement into removal plots demonstrates that in most populations there is a “transient pool”
of animals available to settle in habitat from which residents have been removed. The RFH and
EFH make different predictions as to the way the correlation between resident density and the
proportion of animals in the transient pool should vary with the season. Fairbairn (1978a) noted
that the number of Peromyscus maniculatus captured on a removal grid was significantly
correlated with density on a nearby mark-and-release grid but not with the rate of increase on
the latter. The ratio between captures on the removal grid and the number of animals currently
encountered on a nearby mark-and-release grid (the “recovery ratio” referred to above) was
highest in late fall and early winter when recruitment into the sedentary population was occurring.
The peak in philopatric recruitment of young into Fairbairn’s populations occurred at a time of
maximum density, and at a time when transients were relatively numerous. Both observed
relationships are difficult to reconcile with an EFH model, but both conform to RFH predictions.
The RFH anticipates that variation in immigration rates should be seasonal, and the inverse
of emigration rates, because immigration rates should peak outside the breeding season. De-
mographic studies of immigration are rare. Andrzejewski (1963) reported that immigrant numbers
showed distinct spring and fall peaks in a forested area. Krohne et al. (1984) noted spring
immigration of Peromyscus into an area where there was no overwinter survival, and Sullivan
(1979) noted a burst of recruitment in colonization habitat in clearcut areas in late summer and
early fall. As with removal grids, trends in such seasonally vacated areas probably reflect numbers
of individuals in the transient population rather than rate of immigration into established pop-
ulations. If some of the uncertainties regarding the identification of immigrants on the basis of
body weight at first capture (Dueser et al., 1984) can be resolved, the method might provide
useful insights into immigration, but the approach has many weaknesses (Tamarin, 1984).
110 Rodent Dispersal
Demographically, the RFH is compatible with the view of species populations as composed
of small local groups, most often matrilineal, which are subject to frequent extinction and
replacement (Anderson, 1970, 1980; Lidicker 1985b; Stenseth, 1983). Few studies have been
sufficiently enduring and detailed to test predictions as to extinction rates, but the model is well-
illustrated by the matrilines observed by Armitage (1984) in the yellow-bellied marmot. It may
be that extinction and recolonization play more important roles in dispersal than we have yet
recognized.
Genetic Predictions and Tests
The RFH and EFH differ in their predictions as to the amount of gene flow, the direction of
gene flow, and the pathways by which genetic information travels. The EFH predicts a high
degree of panmixia and a more or less random exchange of genetic information. The RFH
predicts that gene flow is largely one-way: outward from established matrilines, family groups,
and demes occupying patches of favorable habitat. Significant amounts of inbreeding and genetic
drift are anticipated within breeding units, and outbreeding is expected primarily in the founding
of new groups, making founder effect a significant evolutionary factor in the maintenance of
microspatial heterogeneity. Heterozygote frequencies are expected to decline within the life
span of breeding units. It is expected that homozygotes will tend to be in excess in more permanent
habitats and heterozygote frequency will be higher in temporary habitats.
Examples can be found that fit many of the above predictions, but because they are restricted
to relatively few species their generality remains in doubt. The prediction of microspatial sub-
division is supported by results reported in studies of marmots (Schwartz and Armitage, 1981),
prairie dogs (Chesser, 1983), pocket gophers (Patton and Feder, 1978; Zimmerman and Gayden,
1981), Peromyscus maniculatus (Massey and Joule, 1981), Microtus agrestis (Semeonoff and
Robertson, 1968), M. californicus (Bowen, 1982; Lidicker, 1985b), and in some house mouse
populations (Anderson, 1964; Anderson et al., 1964; Petras, 1967a, 1967b, 1967c; Selander, 1970a;
Singleton, 1983) but not in all (Justice, 1962). Myers (1974) found that clumping of electromorphs
was ephemeral in feral Mus inhabiting barley fields plowed and planted at 3-year intervals.
Drift and founder effects have been invoked as explanations of heterogeneity among local
populations in most of the examples cited in the preceding paragraph, offering considerable
support for the RFH vision of gene flow. Reviewing the evidence for both rodents and mammalian
populations in general, Cothran and Smith (1983) found a tendency for concordance between
chromosomal and genic divergence, which they interpreted as evidence for population subdivision
and the influence of drift and inbreeding. In his study of Cynomys ludovicianus, Chesser (1983)
found greater differentiation among populations within regions than among regions, suggesting
that drift, inbreeding, and founder effects operated within regions, while selection operated
across regions.
Drift and inbreeding, predicted by the RFH, should theoretically lead to homozygote fre-
quencies in excess of those predicted by the Hardy-Weinberg model for panmictic populations
of more than a few hundred individuals. The EFH predicts high levels of heterozygosity as a
result of outbreeding. Results have been variable where homozygote and heterozygote frequencies
have been measured. Homozygote excess has been reported in Cynomys ludovicianus (Chesser,
1983), Microtus agrestis (Nygren, 1980), and Thomomys bottae (Patton and Feder, 1981). Some
lociin Marmota flaviventris showed excess heterozygotes and others a slight excess of homozygotes
(Schwartz and Armitage, 1981). Heterozygote excess has been characteristic of some Mus pop-
ulations, but seasonal fluctuation and microspatial variation in heterozygote frequency indicate
that both selection and social organization are involved (Berry and Peters, 1977). The evidence
is compelling that many factors enter into determination of allelic and genotype frequencies
(Berry and Peters, 1977; Peters, 1981; Schnell and Selander, 1981). It appears that some loci
may be affected by drift, whereas selection may over-ride drift at other loci (e.g., Patton and
Feder, 1981). Each locus, each sex, and each seasonal cohort, may be differently affected by
these forces (e.g., see the results obtained by Baird and Birney, 1982a). The relative roles of
Comparisons of RFH and EFH 111
extrinsic factors determining gene flow also remain in doubt, and it is not clear whether im-
migration is made possible because social exclusion of immigrants is ineffective, or because social
stability is frequently disrupted by environmental stresses or catastrophies. Conclusions have also
varied with respect to the relative effect of physical barriers on gene exchange. Zimmerman and
Gayden (1981) observed little evidence that a river interfered with gene exchange in Geomys
bursarius, but Smith and Patton (1984) concluded that physical barriers were of major importance
in Thomomys bottae.
The RFH does not, in the same sense as the EFH, require sex-linked or sex-limited alleles
imparting a tendency to emigrate in order to explain sexual bias in emigratory tendency. Although
residents are expected to vary in their behavior toward offspring and other kin, and in their
aversive behavior toward non-kin, the RFH does not postulate polymorphism in the same sense
as does the EFH.
As anticipated by the RFH, emigrants are unlikely to form a genetically distinctive subset of
the sex-age cohort of the local population from which they originate, and emigrants from any
given local population should be less variable genetically than transients passing through the
area. Shifting patterns in emigration simply reflect the sex-specific tactics of residents in response
to their residual reproductive values and to the varying environment. In this scenario, there
seems to be little need to invoke a “phenotypic plasticity” hypothesis (Lidicker, 1985a) to explain
changing patterns in emigration and immigration.
It is important for comparison of the two hypotheses that we assess the cost-benefit ratio of
inbreeding in natural populations. Demonstration of adaptations that prevent strong inbreeding
favors the EFH, but if the cost of incest is high, residents should avoid inbreeding under the
RFH as well. Absence or ineffectiveness of obstacles to moderate inbreeding are more compatible
with the RFH, and the RFH is therefore supportive of the concept of optimal levels of inbreeding
(Bateson, 1983; Shields, 1982). Studies designed to determine the significance of inbreeding
depression in nature will be of value in testing both the RFH and the concept of optimal breeding
structure. Our traditional acceptance of the negative effects of inbreeding seems to me to be out
of all proportion to the available data from populations in the field.
One of the more effective genetic tests for population structuring might be comparison of
litter sizes or other measures of fitness in intrademe and interdeme crosses. If matrilines or other
population units are inbred, outbred matings should show heterosis; if populations are unstruc-
tured, no increase in fitness should be evident.
If female residents are replaced by their daughters more often than males are replaced by
their sons, populations will be structured into matrilineal clusters upon which selection can act
to produce co-adapted gene complexes. Long distance gene flow will be largely a male prerogative,
but will be limited by restrictions on male ability to penetrate established groups. Maternal
nepotism leading to retention of daughters and an occasional son in the natal range favors
inbreeding. As visualized in the RFH, the major counters to inbreeding are male emigration,
mortality, seasonal delay in maturation of female offspring, environmental instability, and the
long-term instability and frequent extinction of social groups as described by Singleton (1983)
and Pokki (1981). More succinctly, the RFH view is that inbreeding is limited primarily by low
survivorship (Patton, 1985). The degree of inbreeding should be highest in habitats that are
continuously occupied and lowest in habitats where extinction is frequent and colonization is
seasonal or occasional.
In polyestrous seasonal breeders (for example, microtines and many populations of wild house
mice) in continuously occupied habitat, the RFH predicts that the incidence of inbreeding will
show a seasonal pattern, with outbreeding predominating at the beginning of the breeding season
and inbreeding peaking as the females of the first litters become sexually mature and settle in
relatively uncrowded natal habitat. If barriers to immigration break down between breeding
seasons, each season will begin with outcrossing among inbred, overwintered young. Inbreeding
depression in litter size may be eliminated in the first outbred mating (Lynch, 1977). The result
of spring outbreeding could be heterosis, leading to larger litters at a time when new habitats
112 Rodent Dispersal
are available to be colonized and resources are rising toward peak availability. Anderson and
Boonstra (1979) found that embryo counts in overwintered female voles in spring were larger
than those from females of equal weight collected in summer and fall, a relationship that would
be expected if spring matings were heterotic. Seasonal shift in mean heterozygosity of offspring
suggestive of such a pattern has been noted in the field in several other studies (Baird and Birney,
1982a; Kuryshev and Khvorostyanskaya, 1983; Massey and Joule, 1981; Mihok et al., 1983; Myers,
1974; Petras and Topping, 1983). Although they did not carry out an analysis of the correlation
of heterozygote deficiency with the progression of the breeding season, Gaines et al. (1978) noted
that heterozygote deficiency increased as density increased.
Berry and Murphy (1970), Berry and Jakobson (1975), and Berry and Peters (1977) have
reported data that clearly demonstrate seasonal shifts in selection, but also appear to show increase
in heterozygote abundance over the breeding season, contradictory to the seasonal pattern sug-
gested in the preceding paragraph. It is not clear whether their data truly reflect an increase in
outbreeding as the breeding season progressed, or whether they reflect a sampling technique
that failed to discriminate among residents and transient or peripheral individuals. Further
investigations designed to answer that question would be helpful.
Does an annual cycle in inbreeding and outbreeding lend support to the ideas of Charnov
and Finerty (1980) as to variation in relatedness during a multiannual cycle? I think not. If, as
the RFH assumes, kin groups and matrilines are highly impermeable during the breeding season,
effects of multiannual trends in density will be buffered by population structuring, and the effect
visualized by Charnoy and Finerty seems unlikely.
That data on heterozygote frequency are difficult to interpret is illustrated by the study by
Petras and Topping (1983). Two stochastic models were developed, based on characteristics of
corn-crib house mouse populations in Ontario. The models were applied to loci coding for t-allele
and hemoglobin (Hbb). Both models explained the observed frequencies, provided strong selection
pressure favoring Hbb heterozygotes was incorporated in the high-gene-flow model. The authors
concluded that the high-gene-flow model was more realistic, but this required three assumptions:
gene flow must be high because populations were disrupted annually by the emptying of the
corn cribs, there must be selection against +t phenotypes (the evidence is conflicting), and there
must be selection in favor of Hbb heterozygotes.
Mihok et al. (1983) noted that gene pools in Clethrionomys gapperi appeared to be relatively
stable and suggested that this might be explained either by restricted gene flow or by selection.
Although small deme size predisposes local groups to initial genetic instability as a result of drift
and founder effects, inbreeding and maternal nepotism favor sufficient stability so that favorable
alleles and combinations will attain intermediate frequencies at which they will be sufficiently
buffered against drift for selection to operate. As illustrated by the studies of Baker (1981b) and
Myers (1974), immigration (introducing new alleles and increasing recombination) may be largely
dependent on resident mortality and disruption of established groups by periodic disturbance.
The RFH model envisages the exchange of genetic material as constrained by resident exclusion
of immigrants and female nepotism directed primarily toward daughiers. This form of genetic
structuring is best documented among diurnal ground squirrels, but if the RFH is correct it
should be demonstrable in many species of smaller nocturnal rodents as well. The life expectancy
of matrilines probably varies with the life history strategy followed by a population, with the
degree of environmental stochasticism experienced, with habitat quality and with the relative
fitness of the available alleles and allelic combinations.
If residents behave as postulated by the RFH, food supplements should reduce emigration
and encourage inbreeding. Data showing that heterozygosity at the esterase-1 locus in Peromyscus
polionotus was highest in areas where food was less abundant was interpreted by Smith et al.
(1984) to suggest that scarcity of food selected for heterozygotes. The RFH explanation would
be that food supplements increased inbreeding and lowered heterozygosity in the areas where
supplemental food was provided.
Depending to some extent on the stability of demes, clines should be relatively narrow. One
Comparisons of RFH and EFH 113
TABLE 2.—Qualitative comparison of EFH and RFH predictions relative to behavior.
Behavior pattern RFH expectation RFH:EFH trend
Residents
Male-male aggression High >
Male-female aggression Low <
Female-female aggression High >
Probability of adult emigration Low <
Male territoriality Variable >
Female territoriality High >
Resident dominance over transients High >
Male nepotism Low >
Female nepotism High >
Avoidance of incest by female Moderate <
Avoidance of incest by male Low <
Female range shifts at weaning Occasional >
Reciprocal altruism among neighbors High >
Resistance to immigration High >
Kin recognition by females High >
Kin recognition by males Moderate >
Seasonal change in behavior toward young High >
Expulsion of young by males High >
Expulsion of young by females Occasional >
Restraint in contests with young High >
Retention of young as helpers Occasional >
Offspring
Philopatry High >
Cohesive behavior among kin High >
Aggression toward transients Moderate >
Male emigration High >
_ Female emigration Low <
Ratio of male to female emigration High >
Male immigration Low <
Female immigration Moderate <
Ratio of male to female immigration Low <
Male dispersal Low <
Ratio of male to female dispersal Moderate <
Male dispersal distance High >
Female dispersal Low <
Female dispersal distance Low <
Defense of the natal range by offspring Moderate >
Avoidance of incest by females Moderate <
Avoidance of incest by males Low <
such abrupt cline has been investigated in detail in Danish house mouse populations (Selander
et al., 1969a). Where demes are less stable than those of commensal house mice, clines should
be broader.
Genetically based removal studies could be useful in testing the RFH. If immigration and
mate choice are largely determined by resident females, removal of resident females should be
more effective in increasing heterozygosity in a matriline or deme than removal of resident
males. Experimental introduction of individuals carrying marker alleles and monitoring of their
spread (e.g., Anderson et al., 1964; Baker, 1981b) is the ultimate test of immigration, an effective
measure of the effect of structuring on gene flow, and thus an effective means of testing the
validity of the RFH.
The observation that genetic individuality of local groups in Microtus californicus is high
when density of the metapopulation is low, and that this micro-heterogeneity appears to decrease
with increased density, has been taken to imply that panmixia increases with regional density
114 Rodent Dispersal
TABLE 3.—A qualitative comparison of EFH and RFH predictions relative to demography.
Demographic parameter RFH expectation RFH:EFH trend
Dispersion
Random or overdispersed Rare <
Clumped Common >
Kin clusters Common >
Family groups Common >
Matrilineal groups _ Common =
Emigration
Crude rate*
Positively density dependent** Rare <
Negatively density dependent Often >
Seasonally dependent Generally >
Adult male rate
Positively density dependent Occasional <
Negatively density dependent Occasional >
Seasonally dependent Generally >
Adult female rate
Positively density dependent Rare <
Negatively density dependent Occasional >
Seasonally dependent Generally >
Juvenile male rate
Positively density dependent Occasional <
Negatively density dependent Occasional >
Seasonally dependent Generally >
Juvenile female rate
Positively density dependent Occasional >
Negatively density dependent Occasional <
Seasonally dependent Generally >
Immigration
Crude rate Low <
Adult male rate Low <
Adult female rate Low <
Juvenile male rate Low to moderate <
Juvenile female rate Moderate >
Fluctuations in density
Intrademe (local) stability High >
Metapopulation (regional) stability Moderate <
* Proportion of population emigrating irrespective of sex or age.
** Increases with number of individuals/unit area as measured on a conventional trapping grid.
(Bowen, 1982; Lidicker, 1985b). Because the analysis compared grids, rather than matrilines,
the data collected by Bowen (1982) appear to be subject to the alternative interpretation that
the decline in heterogeneity was merely due to the occupation of interstitial habitat by cohorts
of young, rather than an actual increase in outbreeding. The evidence that resistance to immi-
gration increases with density (Hestbeck, 1986; Wolff, 1985a) favors the view that breeding
structure was unaffected, but either interpretation is compatible with the RFH.
The EFH predicts that populations will be integrated by gene flow into relatively large units
with common genetic and demographic characteristics. Such units would tend toward a regional
adaptive compromise, minimal ecotypic or local adaptation, and a relatively high genetic inertia
in the face of environmental change. The RFH differs in respect to each of the above charac-
teristics, and leads to the kind of evolutionary model outlined by Patton (1985) for Thomomys.
Regional metapopulations would be composed of many small, more locally-adapted, and ge-
netically independent groups. In the event of sudden environmental changes some groups would
go extinct and be replaced by colonists exported from other groups in which gene combinations
chanced to be preadapted. Interdemic selection, in this form, could bring about rapid evolutionary
Comparisons of RFH and EFH 115
TaBLE 4.—A qualitative comparison of EFH and RFH predictions relative to genetic structure and
evolutionary processes.
Genetic/evolutionary parameter = RFH expectation RFH:EFH trend
Breeding system
Inbreeding
In general Common >
Seasonal variation General >
Outbreeding
In general Rare <
Seasonal variation General >
The genome
Coadaptation in the genome General >
Neutral alleles Common >
Heterozygote frequency Moderate <q
Genetic structure in populations
Extensive panmixia Unusual <
Local clustering General >
Kin groups and matrilines General >
Genetic neighborhood size Small <
Cline width Narrow <
Processes changing the gene pool
Regional selection General =
Local adaptation General >
Founder effects General >
Drift Common >
Kin selection Common >
Interdemic selection Occasional >
shifts of the type visualized for a self-fertilizing snail by Selander and Hudson (1976) and for
rodents by Shvarts (1977). Sequences of such rapid genetic reorganizations in the metapopulation
could play significant roles in the swift adaptive radiations that appear to characterize rodents
and in the genesis of “punctuations” in evolutionary equilibria.
Krohne and Baccus (1985) suggested that demographic units, defined by demographic ho-
mogeneity (similar sex and age structure and synchronous patterns of fluctuation, extinction,
etc.), are independent of genetic units (demes). I believe this suggestion should be rejected. As
Krohne and Baccus recognize, common demographic patterns are likely to result from common
seasonal changes and habitat characteristics. Demographic similarity of this sort does not reflect
demographic unity, merely operation of similar external pressures on groups that are in fact
independent both genetically and demographically.
The genetic landscape of a species as visualized by the RFH is a little like a restless stream
with transient wavelets erupting in an irregular pattern. As it conforms to the surrounding
environment it can break at times into a braided pattern of independent streamlets. Some
streamlets dissipate in the gravel and disappear, whereas others persist and expand. Most rejoin
the main stream, but occasionally a streamlet may drop into a new channel.
Innovation is favored in a model that incorporates founder effects and drift. Coupled with
resistance to immigration it allows scope for both individual and collective (kin and interdemic)
selection in generating local adaptation. The RFH predicts a genetic and evolutionary landscape
that is dynamic. Individual fitness remains a dominant evolutionary force, but because regional
metapopulations are highly subdivided, new gene combinations may be preserved and persist
long enough to be tested by selection; this advantage of inbreeding is maintained without loss
of individual variation. Kin (and even interdeme) selection, founder effects, and drift may become
effective agents of change. The pattern reflects a reasonable life history strategy for rodent
environments that are spatially and temporally coarse grained and where environmental change
116 Rodent Dispersal
is stochastic. For the metapopulations, such a landscape provides a kind of serendipity, making
it probable that adaptive gene combinations will be available in replicate to meet whatever
environmental variations occur (Anderson, 1978).
Summary
The RFH postulates control of dispersal by resident behaviors. The EFH postulates control
of dispersal by the genes of potential emigrants. My purpose in this chapter has been to stimulate
the imagination of future investigators by suggesting the nature and design of investigations that
challenge the dichotomy I have proposed. Tables 2, 3, and 4 further summarize the differences
between the EFH and RFH. The intention in each of these tables is to indicate the relative trend
or emphasis for a series of observable qualities and to imply that although no single test may
firmly establish one hypothesis or the other, the two differ in emphasis over a wide range of
behavioral, demographic, and genetic topics. The sum of the trends in favor of one or the other,
over the tables as a whole, may be the best indication of the power of the competing views.
A CONCLUDING STATEMENT
I believe that the hypothesis that emigration evolved through a gain in fitness to emigrants is
weak on many counts. In its place I have proposed an alternative that seems to me to be logically
coherent and to be supported by a wide range of observations take from the literature. Never-
theless there is much to be done before one or the other hypothesis can be fully falsified and
the other tentatively accepted. I see it as particularly important that the elements in the central
dogma of the RFH (site tenacity, resident dominance, maternal nepotism, offspring philopatry,
optimization of relatedness in mate choice) be fully tested.
The RFH alternative has far-reaching behavioral, demographic, and genetic implications. I
have tried to suggest predictions that should follow if resident behavior has been selected so as
to maximize fitness through manipulation of young by parents in accordance with the dictates
of inclusive fitness and kin selection, and if young, in their turn, are basically philopatric, but
respond to parental strategies in ways that have been selected according to the same principles.
One cannot doubt that emigration can be induced by a variety of proximal mechanisms (Dobson
and Jones, 1985), but this need not exclude the possibility that evolution has generated a strategy
which characterizes groups with a broad range of life histories. The RFH predicts that emigration
will vary with seasonal and other conditions, and I believe it obviates the need for such concepts
as pre-saturation dispersal and phenotypic plasticity as envisaged by Lidicker (1975, 1985a).
In the area of demography, the RFH emphasizes the responses of female residents to the
resource demands of gestation and lactation as a factor in emigration rates and regulation of
local density, and de-emphasizes male aggression as a factor in limiting population growth. It
predicts that the probability that a potential emigrant will depart from the natal site is almost
entirely independent of density. It requires that analyses of emigration be specific to sex, age,
degree of genetic relationship, season, season of birth, residual reproductive value, and resource
availability.
The RFH is an hypothesis attractive to those who appreciate environmental heterogeneity
and the role of population structuring in buffering population dynamics and limiting gene flow.
Dispersal, as visualized by the RFH, takes place in habitats that are patchy, with favorable
patches supporting discrete, predominantly matrilineal groups of closely related individuals. Less
favorable habitats may be occupied seasonally or intermittently, and may be characterized by
outbreeding. In this respect the RFH relies on models of habitat and population structure similar
to those recently envisioned by a number of investigators (Anderson, 1970, 1980; Hansson, 1977;
Naumov, 1972; Smith et al., 1978; Stenseth, 1983). In temporal terms it also incorporates the
notion that distinctive seasonal generations, as described by Anderson (1970), Martinet (1967),
Reichstein (1964), and Schwarz et al. (1964), are significant in the demographic and evolutionary
dynamics of seasonally breeding polyestrous species. In a general sense, the RFH supports the
supposition of Gaines (1985) that changes in the composition of gene pools are mast likely to be
consequences, rather than causes, of demographic patterns.
The RFH eliminates the need to demonstrate “dispersal genotypes.’ It predicts that emigrants
will be subject to especially intense and variable selective pressures. Although the RFH is based
on individual selection, it suggests trends toward demic population structuring that may be
sufficient to require that selection interact with chance effects in a dynamic equilibrium. In
populations so structured, regional demography and evolution incorporate both the sums and
interactions of local events. The evolutionary process is open to the occasional or even frequent
operation of founder effects followed by inbreeding under local selective pressure, speeding
generation of a diversity of locally adapted demes. Within limits set by the degree to which
117
118 Rodent Dispersal
emigrants outbreed, differential success in survival, expansion, and dissemination ot such local
groups could couple individual, kin, and interdeme selection as defined by Wilson (1973) in
ways that could significantly influence the speed and direction of evolutionary change.
The Resident Fitness Hypothesis expands and extends to rodents in general an analysis initially
applied specifically to microtines (Anderson, 1980). It has been foreshadowed in numerous ways
by the theories, observations, and experiments of a host of investigators. I am indebted to all of
them. As developed here, I believe the hypothesis offers a new, significant, testable, and predictive
model that future studies of behavior, demography, and genetics in rodent populations can
explore.
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INDEX
Acomys sp. (general), 13
Adult (defined), 2
Aggression, 38-40, 68, 73, 74, 90
Altruism, 34
Apodemus sp. (general), 18, 50, 52, 79,
80, 98, 95
Apodemus sylvaticus, 50, 52, 104
Arvicola sp. (general), 117
Arvicola terrestris, 51, 52
Castor canadensis, 95
Chitty-Krebs Hypothesis, 117
Clethrionomys sp. (general), 11, 16, 17,
20, 21, 27, 28, 50-52, 54, 58, 59,
70, 79, 92, 97, 104
Clethrionomys gapperi, 90, 94
Clethrionomys glareolus, 16, 17, 49,
68, 81, 94, 95, 104, 115
Clethrionomys rufocanus, 51, 57, 58,
69, 97
Clethrionomys rutilus, 68
Coadaptation, 22
Confinement syndrome, 98-101
Cohesion (among kin), 55-57
Competition (general), 4, 5, 30, 32, 69-
Th, 1
Cycles, 110
Cynomys ludovicianus, 20, 56, 63
Delayed puberty, 14, 44—46, 66, 67, 78,
93, 94, 97, 98
Dipodomys sp. (general), 77
Dipodomys merriami, 58
Dipodomys spectabilis, 10, 11, 29, 51,
62, 67, 75, 77, 82, 83, 90
Dispersal, 9, 51, 52, 103, 104
terminology, 1-7
general, 9, 51, 52, 103, 104
Dominance, 16, 60, 61, 70, 71
EFH (defined), 10
Emigrant,
defined, 2-3
general, 7, 10, 11, 110
Emigration-prone genotypes, 27, 29
Emigratory stimuli, 82-87, 91
Emigratory tendency, 109, 110
Emigration sink, 5
Eutamias sp. (adult emigration), 50
Evolution (parent-offspring relation-
ships), 30
Field observation (practicality), 110
Fitness (general), 9, 10, 13, 30, 31, 104
Founder effects, 61
Genetics (gene flow, genetic drift), 110-
116
Habitat (general), 32, 33, 52, 75
Heterocephalus glaber, 78
Heterosisis, 61, 62
Heterozygote frequencies, 112
Home range (general), 2, 8, 9, 18, 48-
50, 68, 69, 74-77
Hydrochoerus hydrochaeris, 56
Immigrant (defined), 4
Immigration, 17, 18, 20, 78-82, 98, 109,
lll
Inbreeding (general), 24, 25, 34, 35,
59-67, 108, 109
Inbreeding (avoidance), 22, 24, 26, 60,
64, 72, 73, 98, 105
Inbreeding (depression), 22, 24, 42
Infanticide, 71, 72
Juvenile (defined), 2
Kin selection, 111, 112
Lemmus sp. (general), 11
Lemmus lemmus, 90
Limitation of population density, 38,
89, 41
Marmota calligata, 16, 79
Marmota flaviventris, 15, 19, 20, 56,
59, 64, 68, 93, 96
Mate selection, 17, 40, 57-59
Meriones unguiculatus, 14, 18, 57, 98
Mesocricetus auratus, 16
Microcavia sp. (general), 70, 88
Microgeographic variation, 28, 61
Microtus sp. (general), 6, 17, 27, 28,
49, 54-58, 69-72, 75, 77, 79-84,
89, 92, 108, 112, 113
Microtus agrestis, 21, 61, 75, 84, 85,
88, 89
Microtus arvalis, 51, 56
Microtus californicus, 8, 14, 15, 20, 24,
51, 61, 68, 81, 82, 85, 96, 107
Microtus canicaudus, 65
Microtus montanus, 16, 57-59, 75, 88
Microtus ochrogaster, 14-17, 25, 50-
52, 58, 64, 65, 78, 81, 83, 89, 98,
lll
Microtus oeconomus, 75
Microtus oregoni, 80, 90
Microtus pennsylvanicus, 18-20, 29,
57, 63, 68, 70-78, 81, 91, 96, 107,
108, 118, 114
Microtus pinetorum, 14, 78, 80
Microtus townsendii, 11, 16, 56, 80-
82, 93, 95, 115
Mus sp. (general), 8, 14, 16-19, 55-59,
66, 68, 69, 79, 83, 92-94
Mus musculus, 14, 18, 21, 23
140
Natal range (defined), 1-2
Neotoma sp. (general), 58, 59, 114, 115
Nepotism, 60, 72, 73, 76-78, 105
Notophthalmus viridescens, 9
Ochotona sp. (general), 61
Ochrotomys sp. (general), 75
Onadatra zibethica, 11
Onychomys sp. (general), 72
Outbreeding, 24, 25
Parental disbursement, 6, 35, 36, 104,
105
Parent-offspring conflict, 31-34
Parental investment, 6, 35-37, 71, 105
Parental strategy, 36, 37
Parental investment, 71
Paternity, 71, 72
Peromyscus sp. (general), 5, 16, 22, 24,
00, 51, 54, 58, 65, 66, 72-75, 79-
81, 96, 104, 114, 115
Peromyscus eremicus, 65, 66
Peromyscus gossypinus, 18, 19, 75
Peromyscus leucopus, 12, 14, 19, 51,
do, 56, 59, 61, 62, 73-75, 79-81,
89, 90, 93
Peromyscus maniculatus, 14-16, 19-
23, 49, 55, 88-90, 98, 108, 118
Peromyscus polionotus, 55, 56, 62
Philopatry, 5, 10-14, 32, 41, 42, 50-52,
62, 107-110
Population structure, 9, 116
Pregnancy block, 41, 45
Probability of dispersal, 25
Proportional representation of parental
genomes, 34, 35
Rattus sp. (general), 55, 72
Rattus norvegicus, 13, 14, 20, 70, 71
Recruitment, 59, 77
Relatedness, 109
Removal studies, 108
Replacement rate (“recovery ratio’),
111
Index 141
Resident (defined), 2
Resource manipulation, 108, 109
Resident pressure (responses of young),
92-94, 96-98
Reithrodontomys sp. (general), 79
Relatedness, 31
RFH (defined), 29, 30
Sigmodon hispidus, 11, 12
Social discrimination, 52-55, 58
Social fence hypothesis, 107-111
Spalax sp. (general), 61
Spalax ehrenbergi, 59
Spermophilus sp. (general), 53, 54, 56,
Spermophilus beldingi, 20, 51, 52, 56,
86, 87
Spermophilus columbianus, 56, 76, 77
Spermophilus elegans, 96, 97
Spermophilus parryi, 56
Spermophilus richardsonii, 13, 53, 62,
68, 76, 90
Spermophilus tridecemlineatus, 68, 70
Strategies (general), 33, 34, 37-39, 41-
44, 46, 47, 92
Subadult (defined), 2
Supplemental food, 74, 90, 91
Tamias sp. (general), 70
Tamias striatus, 79
Tamiasciurus sp. (general), 18, 77, 80
Territoriality, 6, 38, 69, 70, 72-74
Thomomys sp. (general), 67
Thomomys bottae, 61
Transient,
defined, 3, 4
general, 11, 12, 17, 94, 95
Transiency and pregnancy, 17, 18
Transient pool, 27, 28, 117
Variance (in male reproductive suc-
cess), 70, 71
Weanling (defined), 1
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Date Due
DEC 2 1 2001
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