TEXAS TECH UNIVERSITY
Natural Science Research Laboratory
Occasional Papers
Museum of Texas Tech University
Number 277 2 October 2008
Phylogenetics of the Fruit-eating Bats (Phyllostomidae: Artibeina)
Inferred from Mitochondrial DNA Sequences
Steven R. Hoofer, Sergio Solari, Peter A. Larsen, Robert D. Bradley, and Robert J. Baker
Abstract
Approximately 24 species classified in three groups ( Artibeus , Dermanura , and Koopma¬
nia ) compose Subtribe Artibeina, an assemblage of New World leaf-nosed bats (Phyllostomidae)
for which evolutionary relationships have proven difficult to resolve. We examined artibeine
systematics through broad taxonomic sampling and phylogenetic analysis of DNA sequences
for two mitochondrial genes. Analysis of 16S rRNA sequences offered an additional test of
previous genealogical hypotheses, and facilitated knowledge about the congruence in variation
between the well studied cytochrome-6 gene and the evolutionary history of this complex of
bats. Our results illustrate a high degree of congruence between these linked mitochondrial loci
that in combination offers a well resolved gene tree and robust predictions to all but a few of
the examined relationships. Highlights include: monophyly of Artibeina in contrast to previous
hypotheses of polyphyly; two main lineages within Artibeina in accordance with monophyly
of the smaller Dermanura species and larger Artibeus species; sister relationship between A.
concolor and other Artibeus species rather than with Dermanura , contrasting the argument for
recognizing A. concolor as a separate genus ( Koopmania ); reconfirmation of several species
formerly considered subspecies (A. planirostris , A. schwartzi, D. bogotensis, D. rava, and D.
rosenbergi)-, and further indication that A. intermedins and A. lituratus are conspecific.
Key words: 16S rRNA, Artibeus , cytochrome-6, Dermanura , DNAsequence, Koopmania ,
phyllostomid bats, systematics
Resumen
Aproximadamente 24 especies pertenecientes a tres grupos ( Artibeus , Dermanura , y
Koopmania ) componen la subtribu Artibeina, un ensamblaje de murcielagos de hoja nasal del
Nuevo Mundo (Phyllostomidae), cuyas relaciones evolutivas han sido dificiles de resolver. Ex-
aminamos la sistematica de los artibeinos a traves de un amplio muestreo taxonomico y analisis
filogeneticos de secuencias del ADN para dos genes mitocondriales. Analisis de secuencias del
gen 16S rARN ofrecen una prueba novedosa de hipotesis genealogicas previas, facilitando el
conocimiento sobre la congruencia en variacion respecto al mejor conocido citocromo b y la
2
Occasional Papers, Museum of Texas Tech University
historia evolutiva de este complejo de especies. Nuestros resultados ilustran un alto grado de
congruencia entre estos loci mitocondriales, que en combinacion ofrecen predicciones robustas
para casi todas las relaciones examinadas. Resultados relevantes incluyen: monofilia de los Ar-
tibeina en contraste a hipotesis previas de parafilia; dos linajes mayores dentro de los Artibeina,
correspondiendo con la monofilia de especies pequenas de Dermanura y grandes de Artibeus',
la relacion cercana entre A. concolor y otras especies de Artibeus antes que con Dermanura,
en contraste con la propuesta de reconocer A. concolor como un genero distinto ( Koopmania );
el reconocimiento de varias especies previamente consideradas subespecies (A. planirostris, A.
schwartzi, D. bogotensis, D. rava, y D. rosenbergi)', y el reconocimiento d eA. intermedius como
un sinonimo menor de A. lituratus.
Palabras clave: 16S rARN, Artibeus', citocromo-#; Dermanura', filostomidos; Koopmania',
murcielagos; secuancias de ADN; sistematica
Introduction
Artibeine bats compose a large and diverse group
of fruit-eating specialists within the New World family
Phyllostomidae (subfamily Stenodermatinae: subtribe
Artibeina — Baker et al. 2003). From 18 to 24 species
are recognized (Simmons 2005; Larsen et al. 2007;
Solari et al. in prep.) and classified into three groups:
the medium- to large-sized species of Artibeus ( amplus,
fimbriatus, fraterculus, hirsutus, inopinatus, interme¬
dius, jamaicensis, lituratus, obscurus, planirostris,
and schwartzi), the small-sized species of Dermanura
(i anderseni, azteca, bogotensis, cinerea, glauca, gnoma,
incomitata,phaeotis, rctva, rosenbergi, tolteca, and wat-
soni ); and the medium-sized Koopmania {concolor).
Morphologically, Enchisthenes hartii shares affinities
with Artibeus and also has been recognized as part of
the artibeines (e.g., Koopman 1993, 1994).
Relationships among artibeine bats have proven
difficult to resolve with the characters that have
been examined so far (morphology, karyotypes, and
cytochrome-# DNA sequences). As a result, there are
disagreements over rank status of Dermanura and Arti¬
beus and over monophyly of the group as a whole. For
example, Owen’s (1987, 1991) analyses of mensural
and discrete-state morphological characters indicated
a polyphyletic origin for Artibeina: Artibeus shared
a most recent common ancestry with Ectophylla and
Uroderma (his subtribe Artibeini) whereas Dermanura
and Koopmania shared a most recent common ancestry
with Enchisthenes and the white-shouldered stenoder-
matine genera {Ametrida, Ardops, Ariteus, Stenoderma,
Centurio, Phyllops, Pygoderma, and Sphaeronycteris).
In contrast, analyses of cytochrome-# DNA sequences
and EcoRI-defined satellite DNA demonstrated a most
recent common ancestry for Artibeus, Dermanura, and
Koopmania (monophyly of Artibeina; Van Den Bussche
et al. 1993, 1998). Based on anagenic and cladogenic
interpretations of their results, coupled with morpho¬
logical and karyotypic evidence (Andersen 1906; Baker
1973; Straney et al. 1979), Van Den Bussche et al.
(1993, 1998) recognized Artibeus and Dermanura as
separate, closely related genera, and Koopmania con¬
color as A. concolor. The monotypic Enchisthenes was
regarded as genus distinct from Artibeina, which has
been affirmed in additional studies of morphological
and molecular data (Baker et al. 2000, 2003; Wetterer
et al. 2000).
Although the Van Den Bussche etal. (1993,1998)
studies are the most important and comprehensive mo¬
lecular assessments of Artibeine relationships to date,
their taxonomic sampling was limited at that time by
the lack of available tissue samples for Artibeus and
Dermanura and lack of efficient methods of automated
DNA sequencing. Tissue samples of numerous addi¬
tional individuals for the taxa they examined, as well as
several newly recognized species (A. schwartzi [Larsen
et al. 2007] and D. rava and D. rosenbergi [Solari et
al. in prep.]), are now available for molecular study.
Also available (and feasible) now are contemporary
phylogenetic methods that utilize objective systems for
character weighting and efficient systems with which to
reconcile important biological phenomena for molecu¬
lar data (e.g., among-site rate variation, unequal base
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
3
frequencies, and nonindependence of substitutions).
Therefore, our purpose in this study was to re-assess
monophyly of Artibeus, Dermanura , and Artibeina, as
well as the validity of Koopmania, through broad taxo¬
nomic sampling and phylogenetic analysis of complete
cytochrome-# sequences along with a complementary
dataset of complete 16S ribosomal RNA (rRNA) se¬
quences. These linked genes together should increase
the probability of detecting supported resolution to the
gene tree (Moore 1995).
Materials and Methods
Specimens examined. —Specimens examined are
listed in the Appendix, including information associ¬
ated with museum vouchers. We generated complete
cytochrome-# sequences for 37 individuals and com¬
plete 16S rRNA sequences for 50 individuals. From
GenBank, we retrieved 41 cytochrome-# sequences
that were originally generated by Van Den Bussche et
al. (1993), Lim et al. (2004), Porter and Baker (2004),
Hoofer and Baker (2006), and Larsen et al. (2007), and
six 16S rRNA sequences that were originally generated
by Van Den Bussche and Hoofer (2000) and Baker et
al. (2003). Lists of specimens examined including
voucher information are accessible in each of those
publications and in the Appendix. We used sequences
representing Chiroderma , Ectophylla , and Uroderma
as outgroups (Baker et al. 2000, 2003; Wetterer et al.
2000) and inferred relationships among ingroup taxa
representing Enchisthenes and all recognized species of
Artibeina excepting D. incomitata , for which samples
were unavailable.
Molecular methods. —We extracted genomic
DNAfrom skeletal muscle or organ tissue samples with
standard phenol methods (Longmire et al. 1997). We
followed previous methods to amplify and sequence
the entire cytochrome-# (Larsen et al. 2007) and 16S
rRNA (Van Den Bussche and Hoofer 2000) genes. We
sequenced both strands by using Big-Dye version 3.1
chain terminators, followed by electrophoresis on a
3100-Avant Genetic Analyzer (Applied Biosystems,
Foster, City, California). We assembled resulting, over¬
lapping fragments in AssemblyLIGN™ 1.0.9 software
(Oxford Molecular Group PLC, Oxford, United King¬
dom) and Sequencing Analysis 3.4.1 software (Applied
Bio systems, Inc., Foster City, California).
Phylogenetic analysis. —We performed multiple
sequence alignment for both data sets in Clustal X soft¬
ware (Thompson et al. 1997) with default parameters
for costs of opening and extending gaps. We viewed
alignments in MacClade software (version 4.05; Mad-
dison and Maddison 2002) to ensure there were no
insertions, deletions, or stop codons in the cytochrome-
# sequences and to inspect gap placement in the 16S
rRNA sequences. We delimited ambiguously aligned
sites in the 16S rRNA alignment by using criteria and
justification in Hoofer and Van Den Bussche (2003),
and performed data analysis without those sites. We
coded nucleotides as unordered, discrete characters,
gaps as missing data, and multiple states as polymor¬
phisms. In PAUP* software (test version 4.0bl0; Swof-
ford 2002), we examined level of phylogenetic signal
via the ^-statistic (Hillis and Huelsenbeck 1992) for
100,000 randomly drawn trees.
We inferred phylogenetic relationships by Bayes¬
ian analysis implemented in MrBayes 2.01 software
(Huelsenbeck and Ronquist 2001) and by Maximum
Likelihood and Parsimony analyses implemented
in PAUP* software (test version 4.0b 10; Swofford
2002). The general time reversible (GTR) model with
allowance for gamma distribution of rate variation (T)
and for proportion of invariant sites (I) best fit both
cytochrome-# and 16S rRNA data based on Akaike
Information Criterion tests implemented in Modeltest
3.06 software (Posada and Crandall 1998).
For Bayesian analysis, we ran two X 10 6 gen¬
erations with one cold and three incrementally heated
Markov chains, random starting trees for each chain,
and trees sampled (saved) every 100 generations. We
treated model parameters as unknown variables (with
uniform priors) to be estimated in each Bayesian analy¬
sis (Leache and Reeder 2002). We ran three indepen¬
dent analyses with burn-in values based on empirical
evaluation of likelihoods converging on stable values.
We calculated a 50% majority-rule consensus tree from
the sample of stabilized trees in PAUP* software (test
4
Occasional Papers, Museum of Texas Tech University
version 4.0bl0; Swofford 2002) and obtained branch
lengths via the “sumt” option in MrBayes software
(Huelsenbeck and Ronquist 2001). We assessed clade
reliability via posterior probabilities and regarded
values > 0.95 as significant.
For Maximum Likelihood analyses, we used the
GTR + T +1 model and parameters given by Modeltest
(cytochrome-#, r AC = 2.42, r AG = 19.70, r AT = 2.99, r CG
0.69. r CT = 41.75, nA= 0.31, jtC = 0.30, jtG = 0.12, a =
1.27, and P = 0.55; 16S rRNA, r Ar = 3.99, r AP = 15.62,
r AT = 4.45, r = 0.76, r rT = 80.08, jtA= 0.37, jtC = 0.20,
jtG = 0.18, a = 0.76, and P inv = 0.58), performed full
heuristic searches with 10 random additions, starting
trees by simple addition, tree-bisection-reconnection
branch swapping, and allowance for negative branch
lengths. For Parsimony analysis, we treated all char¬
acters and substitution types with equal probability
and conducted full heuristic searches with 10 random
additions, starting trees by simple addition, and tree-
bisection-reconnection branch swapping. We assessed
clade reliability via bootstrapping with 250 iterations
for Parsimony analyses (Felsenstein 1985) and regarded
values > 70 as support. Due to computation time, we
performed Maximum Likelihood bootstrapping only
on the combined mitochondrial dataset and utilized
a “fast” stepwise-addition approach to tree searching
rather than a full-heuristic search.
Results
Cytochrome- b and 16S rRNA .—Sequence
alignment of the complete cytochrome-# gene for 37
specimens generated in this study (GenBank accession
nos. FJ179223-FJ179259) and the 41 retrieved from
GenBank was unequivocal and without internal stop
codons. Of the 1,140 characters, 697 were constant
and 380 parsimony-informative, with nucleotide varia¬
tion distributed across codon positions as expected for
protein coding genes (Simon et al. 1994): 84 at first
positions, 34 at second positions, and 325 at third
positions. Complete sequences of the 16S rRNA gene
averaged 1,559 base pairs for the 56 taxa examined
(GenBank accession nos. FJ179173-FJ179222),
ranging from 1,557 (A. fraterculus , A. inopinatus,
A. schwartzi, D. anderseni, and D. cinerea ) to 1,562
( D. watsoni). Sequence alignment resulted in 1,578
characters, corresponding in length and similarity to
other 16S rRNA sequences in GenBank. We excluded
83 characters in nine regions of the alignment (rang¬
ing from two base pairs to 46 base pairs) because of
ambiguity in assessment of positional homology. This
left 1,495 characters for analysis, of which 1,110 were
constant and 289 parsimony-informative. Levels of
phylogenetic signal were significant based on the g T
statistic (P < 0.01—Hillis and Huelsenbeck 1992) for
cytochrome-# (-0.3335) and 16S rRNA (-0.3428).
For cytochrome-# and 16S rRNA data sets,
Bayesian likelihoods reached stationarity before
100,000 generations (i.e., bum-in = 1,000), thinning the
data points to 19,000 for each data set. Topology and
posterior probabilities for nodes and model parameters
for all sets of runs (three mns each) within data sets
agreed regardless of choice of outgroup. Maximum
Likelihood analysis resulted in a single best tree for
both cytochrome-# (Lnl = -10,611.03) and 16S rRNA
(Lnl = -8,986.50) data sets. Parsimony analysis re¬
sulted in 240 most-parsimonious trees (length = 2,077,
Cl = 0.28, RI = 0.74) and 108 most-parsimonious trees
(length = 1,125, Cl = 0.46, RI = 0.77) for cytochrome-#
and 16S rRNA data sets, respectively. For both datasets,
differences among most-parsimonious trees primarily
involved alternative arrangements of terminal branches
within species and, in a few instances, involved alter¬
native inter-specific relationships within Artibeus and
Dermanura. Overall, there were some topological
differences within and between data sets and between
the three optimality criteria; however, none of the
differences were supported. Statistically supported
topologies (i.e., > 70% bootstrap value, > 0.95 Bayes¬
ian posterior probability) obtained from all optimality
criteria agreed within and between each data set (Figs.
1 and 2).
Combined cytochrome-b and 16S rRNA. —We
combined the data sets because there was high degree
of congruence and no supported conflicts between
them (Wiens 1998). The combined data set (2,635
base pairs) included the 49 specimens shared between
data sets. It also consists of three chimeric taxa that,
in both cases, included cytochrome-# data from one
specimen and 16S rRNA data from another speci-
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
5
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A. lituratus
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A. fimbriatus
A. fraterculus
A. hirsutus
A. inopinatus
A. concolor
D. bogotensis
D. gnoma
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D. rava
D. anderseni
D. cinerea
D. azteca
D. phaeotis
D. tolteca
D. watsoni
D. rosenbergi
Ectophylla
Enchisthenes
Chiroderma
Uroderma
Figure 1. Maximum likelihood phylogram (Lnl = -10,611.03) from analysis of complete cytochrome-6 sequences
(1,140 base pairs) using best-fit model (GTR + T + I; r AC = 2.42, r AG = 19.70, r AT = 2.99, r CG = 0.69, r CT = 41.75, jtA
= 0.31, jtC = 0.30, jtG = 0.12, a = 1.27, and P mv = 0.55). We designated Chiroderma, Ectophylla, and Uroderma as
outgroups. Numbers above branches are Bayesian posterior probabilities, whereas those below are bootstrap percentages
from Parsimony. Values are shown only for nodes supported by P > 0.95 or bootstrap percentage > 50, or both. “A ”
= Artibeus, “D. ” = Dermanura.
6
Occasional Papers, Museum of Texas Tech University
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D. azteca
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— Ectophylla
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— Uroderma
Figure 2. Maximum likelihood phylogram (Lnl = -8,986.50) from analysis of complete 16S rRNA sequences (1,495
base pairs) using best-fit model (GTR + r +1; r AC = 3.99, r AG = 15.62, r AT = 4.45, r CG = 0.76, r CT = 80.08, jtA = 0.37, jtC
= 0.20, jtG = 0.18, a = 0.76, and P inv = 0.58). We designated Chiroderma , Ectophylla , and Uroderma as outgroups.
Numbers above branches are Bayesian posterior probabilities, whereas those below are bootstrap percentages from
Parsimony. Values are shown only for nodes supported by P > 0.95 or bootstrap percentage > 50, or both. “A.” =
Artibeus, “ D = Dermanura.
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
7
men; Artibeus obscurus comprised two individuals,
Enchisthenes hartii comprised two individuals, and
Chiroderma comprised two species (C. salvini and C.
villosum). Bayesian likelihoods reached stationarity
before 100,000 generations as above, and topology and
posterior probabilities for nodes and model parameters
for all sets of runs (three runs each) agreed regardless
of outgroup choice. Maximum Likelihood analysis
resulted in a single best tree (Lnl= -15,882.18) and
Parsimony analysis resulted in two most-parsimonious
trees (length = 2,769, Cl = 0.38, RI = 0.71). Topolo¬
gies and levels of nodal support obtained from all three
optimality criteria were nearly identical (Fig. 3).
Discussion
Higher-level relationships. —Few assessments of
artibeine relationships have been undertaken that in¬
cluded explicit phylogenetic analysis of Enchisthenes,
A. concolor (= Koopmania), and multiple representa¬
tives of Artibeus and Dermanura. Morphological
studies by Owen (1987, 1991) and molecular studies
by Van Den Bussche et al. (1993, 1998) are the most
comprehensive and reveal competing hypotheses of
relationship. Whereas Owen’s analyses of essentially
all stenodermatine taxa indicate independent origins
for the small- and large-sized artibeine bats, those of
Van Den Bussche et al. support a recent common an¬
cestry for these taxa after diverging from Enchisthenes
and other stenodermatine genera. Resolving these
differences is key to the higher-level systematics and
taxonomy of artibeine bats.
Without Owen’s hypothesis of polyphyly, which
led to him to recognize genus Artibeus (mid- to large¬
sized species), elevate Dermanura (small-sized species)
to generic rank, and describe a new genus Koopmania
(mid-sized A. concolor ), rank status of the three lin¬
eages within Artibeina are arbitrary. This situation has
been acknowledged by several authors, as exemplified
in the most recent classificatory synthesis recognizing
monophyly of the group as a whole and classifying all
three lineages within genus Artibeus (Simmons 2005).
Further, the distinction of Enchisthenes and its distant
relationship to the artibeine bats is well documented
(e.g., Andersen 1906; Van Den Bussche et al. 1993;
Baker et al. 2000; Wetterer et al. 2000).
Our separate and combined analyses of cyto¬
chrome-^ and 16S rRNA sequences strongly support
a clade containing all sampled individuals referable to
Artibeus, Dermanura, and Koopmania to the exclusion
of other sampled stenodermatine genera, including
Enchisthenes (Figs. 1-3). This study therefore affirms
previous cladistic analyses for supporting a recent
common ancestry and monophyly of Artibeina (sensu
Baker et al. 2003) in contrast to Owen’s (1987, 1991)
hypothesis of polyphyly. If our analyses supported the
latter hypothesis, then Artibeus would be depicted as
sharing a most recent common ancestry with Ectophylla
and the other vampyressine genera ( Chiroderma, and
Uroderma), and Dermanura and Koopmania would
be depicted as sharing a most recent common ances¬
try with Enchisthenes. All of our results exclude that
hypothesis.
Although the phylogenetic position of Enchis¬
thenes is not fully resolved, our analyses demonstrate
its anagenic and cladogenic distinction relative to the
artibeine bats. Thus, our results affirm previous studies
of morphological, karyotypic, allozymic, and molecular
data supporting the generic distinction of Enchisthenes
(Andersen 1906,1908; Miller 1907; Baker et ah 1979,
2000,2003; Koop and Baker 1983; Owen 1987,1991;
Van Den Bussche 1992; Van Den Bussche et ah 1993,
1998; Pumo et ah 1996; Tandler et al. 1997; Wetterer
et al. 2000) and disagree with suggestions of recogniz¬
ing E. hartii as a congener of Artibeus (e.g., Koopman
1985,1993,1994; Jones etal. 2002). We follow Baker
et ah (2003) in recognizing E. hartii in its own subtribe
Enchisthenina separate from subtribes Artibeina, Ecto-
phyllina, and Stenodermatina.
Within Artibeina, our analyses indicate two main
lineages in accordance with monophyly of the smaller
Dermanura species and larger Artibeus species. Arti¬
beus concolor is sister to the large species of Artibeus
rather than sister to Dermanura (Figs. 1-3). Although
these relationships received different levels of statistical
support in the separate analyses of cytochrome-# and
8
Occasional Papers, Museum of Texas Tech University
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-TK104116
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TK104592
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- TK18790
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A. intermedius/
A. lituratus
A. planirostris
| A. schwartzi
| A. obscurus
| A. jamaicensis
A. fraterculus
| A. hirsutus
A. inopinatus
— A. concolor
D. bogotensis
| D. gnoma
| D. glauca
D. rava
— D. anderseni
— D. cinerea
D. tolteca
| D. phaeotis
D. azteca
| D. rosenbergi
— D. watsoni
- TK16395 - Ectophylla
- TK22690 / TK55331 — Enchisthenes
-TK46006 - Uroderma
TK25052 / TK70524 — Chiroderma
Figure 3. Maximum likelihood phylogram (Lnl = -15,882.18) from analysis of combined cytochrome-# and 16S
rRNA sequences (2,635 base pairs) using best-fit model (GTR + T + I). We designated Chiroderma, Ectophylla,
and Uroderma as outgroups. Numbers above branches are Bayesian posterior probabilities, whereas those below
are bootstrap percentages from Maximum Likelihood and Parsimony, respectively. Values are shown only for nodes
supported by P > 0.95 or bootstrap percentage > 50, or both. “A” =Artibeus, “D.” = Dermanura.
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
9
16s rRNA sequences, they were depicted in all analy¬
ses and highly supported in the combined sequence
analysis (Fig. 3). As with previous morphological,
karyotypic, allozymic, and molecular evidence (Baker
1973; Straney etal. 1979; Van Den Busscheetal. 1993,
1998; Wetterer et al. 2000), our results provide no sup¬
port to the objective argument of polyphyly that Owen
(1991) used to justify recognizing A. concolor in the
genus Koopmania. We therefore follow the suggestion
of Van Den Bussche et al. (1998) and the classifica¬
tion of Baker et al. (2003) in recognizing Koopmania
concolor as Artibeus concolor.
Although the genetic distinction and sister-taxon
relationship between Artibeus and Dermanura is dem¬
onstrated in this and other studies, taxonomic status
for the two lineages as subgenera within Artibeus or
as distinct genera is a matter of subjective ranking.
Several authors have discussed this issue and ranked the
lineages differently (e.g., Van Den Bussche et al. 1998;
Baker et al. 2000,2003; Wetterer et al. 2000; Lim et al.
2004). Lim et al. (2004) noted that the smaller Der¬
manura species and larger Artibeus species cannot be
diagnosed 100% on the basis of size alone because there
is overlap in forearm length measurements between D.
aztecus (41-49 mm) and two species of Artibeus ( con¬
color , 45-51 mm; inopinatus, 48-53 mm). Lacking any
diagnostic morphological characters, they recognized
the two lineages as subgenera within Artibeus. Wet¬
terer et al. (2000) also recognized them as subgenera
(and Koopmania ) within Artibeus because at that time
there was no convenient way to refer to these taxa as a
monophyletic group if generic status was applied. On
the other hand, Solari et al. (2007) noted that Artibeus
and Dermanura could be diagnosed on the basis of
wing coloration and dental features.
We treat Artibeus and Dermanura as separate
genera within the subtribe Artibeina following the
classification of Baker et al. (2003). This nomencla-
tural arrangement facilitates convenient reference to
monophyly of the group as whole, recognition of both
similarities and differences within it, and additional
subgeneric classification within Artibeus and Derma¬
nura if warranted by future studies (see also Solari et
al. in prep, for additional arguments). Based on our
results, the latter situation seems likely after contem¬
porary revisions are made of each genus with more
data and taxa. Our arrangement also makes sense in
terms of a molecular timescale of divergence of steno-
dermatine genera. According to Baker et al. (in litt.),
Artibeus and Dermanura diverged in the Late Miocene
(6.3 mya) along with most of the vampyressine genera
( Chiroderma , Mesophylla , Platyrrhinus, Uroderma,
Vampyressa, Vampyriscus , and Vampyrodes), predat¬
ing the Pliocene divergence of the white-shouldered
stenodermatine genera ( Ametrida , Ardops, Ariteus,
Stenoderma, Centurio, Pygoderma, and Sphaeronyc-
teris). This divergence estimate fits the criteria for
genus ranking in the Age Related Classification system
proposed for Euprimate taxa (Goodman et al. 1998).
Relationships within Artibeus and Dermanura.—
Sister group relationships and alpha taxonomy within
Artibeus and Dermanura continue to be conjectural,
and full revisions incorporating morphological and
molecular data are warranted for both genera. Although
not a primary focus of this study, the 16S rRNA data
set offers robust resolution to and new insight into
sister group relationships and questions of alpha tax¬
onomy that have been debated in the morphological
and cytochrome-# literature. We briefly discuss some
of them.
Results from new cladistic analyses of morphol¬
ogy and cytochrome-# sequences, focusing on species
diversity within the enigmatic A.jamaicensis complex,
have recommended species recognition for three of the
13 subspecies within A.jamaicensis (Simmons 2005):
planirostris (Patten 1971; Lim 1997; Guerrero et al.
2004; Lim et al. 2004; Larsen et al. 2007), schwartzi
(Larsen et al. 2007); and triomylus (Guerrero et al.
2004; see also Larsen et al. 2007). Our analyses include
specimens referable to planirostris and schwartzi (but
not triomylus). In both cases, results from 16S rRNA
analysis mirror those from cytochrome-# in this and
other studies, yet they provide even more robust sup¬
port to the branching order. Our 16S rRNA results are
best interpreted as evidence for species recognition of
A. planirostris and A. schwartzi as opposed to subspe¬
cies within A. jamaicensis. In avoiding paraphyletic
taxa, the latter would require the synonymy of at least
three other species within A. jamaicensis ( amplus ,
lituratus , and obscurus). Thus, our 16S rRNA results
affirm several studies of cytochrome-# for recognizing
A. planirostris (Guerrero et al. 2004; Lim et al. 2004;
Larsen et al. 2007), and affirm the suggestion by Larsen
et al. (2007) for recognizing A. schwartzi.
10
Occasional Papers, Museum of Texas Tech University
Our mtDNA data, along with those of Larsen
et al. (2007) and Lim et al. (2004), document a well
supported sister relationship between the clade com¬
posed of A. fraterculus, A. inopinatus, and A. hirsutus
and that of A. jamaicensis, A. lituratus, A. obscurus,
A. planirostris , and A. schwartzi (Figs. 1, 2, 3). This
observation has biogeographic significance, supporting
the hypothesis of Patterson et al. (1992) for an histori¬
cal connection between the biota of Middle America
and Western Andean Slope. Artibeus inopinatus and
A. hirsutus are distributed in xeric regions along the
western and southern coasts of Middle America and
their closest South American relative, A. fraterculus,
is distributed in dry regions of southern Ecuador and
northern Peru west of the Andes Mountains. The
remaining species of Artibeus are sister to these xeric
adapted species, and represent a South American radia¬
tion within the genus.
Results from 16S rRNA analysis also affirm
previous morphological (Marques-Aguiar 1994) and
cytochrome-6 (Van Den Bussche et al. 1998; Lim et al.
2004) analyses that suggested recognizing A. interme-
dius as a junior synonym of A. lituratus. Average 16S
rRNA sequence distance between A. intermedius and
A. lituratus (0.81%) is nearly equivalent to the average
distance within other Artibeus species (0.78%) and
much less than that observed between species (4.62%).
These results are of course provisional given the fact
that we examined 16S rRNA sequences from just two
individuals of intermedius (from Copan, Honduras) and
three individuals of lituratus (from western Ecuador
and Union Island, St. Vincent and the Grenadines).
However, they agree with the cytochrome-6 results
from this and other studies that included more indi¬
viduals. Therefore, we follow Marques-Aguiar (1994)
in recognizing A. intermedius as a junior synonym of
A. lituratus pending further study of combined mor¬
phological and molecular characters for populations
of intermedius and lituratus , including those from the
hypothesized region of sympatry in Middle America
(Davis 1984; Marques-Aguiar 1994).
Even fewer cladistic analyses have been under¬
taken examining species diversity within Dermanura
(morphology, Owen 1991; cytochrome-6, Van Den
Bussche et al. 1998). A new study by Solari et al.
(in prep.), incorporating both morphological and
cytochrome-6 analyses and dense taxonomic and geo¬
graphic sampling, recommended species recognition
for D. bogotensis and D. rosenbergi, former junior
synonyms of D. glauca, and species recognition for
D. rava, a former junior synonym of D. phaeotis. Our
analyses include specimens referable to all of these
taxa. In each case, our results from 16S rRNA analysis
mirror those from cytochrome-6 in this study and Solari
et al. (in prep.), supporting a sister relationship between
D. bogotensis and D. gnoma, another between D. rosen¬
bergi and D. watsoni, and a clade containing D. rava,
D. anderseni, and D. cinerea. Our 16S rRNA results
are best interpreted as evidence for species recognition
of D. bogotensis and D. rosenbergi, rather than junior
synonyms oLD. glauca, and species recognition forD.
rava, rather than a junior synonym of D. phaeotis. To
avoid paraphyletic taxa, the alternative classification
(Simmons 2005) would require synonymizing from
one to nine other species and major taxonomic rear¬
rangement. Thus, we follow Solari et al. (in prep.) in
recognizing 12 species within Dermanura, the nine
listed in Simmons (2005; we did not sample incomitata )
plus D. bogotensis, D. rava, and D. rosenbergi.
Our hypotheses of relationship for species di¬
versity and species groups within Dermanura depart
significantly from previous hypotheses for the genus,
including Handley (1987). Like cytochrome-6, our
16S rRNA results correspond with geographic origin
of Dermanura species better than with morphological
similarity. Accordingly, we conclude that our system¬
atic and taxonomic hypotheses better reflect actual
phyletic relationships rather than adaptive similar¬
ity. This is evidenced by biogeographic patterns in
the Dermanura phylogeny that correspond well with
diversification patterns hypothesized for Artibeus as
well as other vertebrates (see Solari et al. in prep, for
discussion of Dermanura phylogeography).
In summary, our phylogenetic analysis of
cytochrome-6 data includes fairly dense and complete
taxonomic sampling for both genera and most recog¬
nized species within them. More importantly, analysis
of 16S rRNA sequences offers a new test of previous
hypotheses about shared common ancestry, sister group
relationships, and alpha taxonomy, thereby facilitating
knowledge about the congruence in variation between
the well studied cytochrome-6 gene and the evolution¬
ary history of bats within Artibeus and Dermanura. Our
results illustrate a high degree of congruence between
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
11
these linked mitochondrial loci that in combination
offer a well-resolved gene tree and robust predictions
to all but a few of the examined relationships (Fig. 3).
Testing the mtDNA phylogeny with independent nucle¬
ar gene sequences and broad taxonomic sampling are
highly desirable to further advance our understanding
of the systematics and taxonomy of artibeine bats.
Acknowledgments
We thank the following persons and institutions
for their generosity in loaning tissue samples and as¬
sistance in locating voucher specimens: Nancy Sim¬
mons of the American Museum of Natural History;
Suzanne McLaren of the Carnegie Museum of Natural
History; Victor Pacheco and Carlos Tello of the Museo
de Historia Natural, Universidad Nacional Mayor de
San Marcos, Peru; Terry Yates and Cheryl Parmenter
of the Museum of Southwestern Biology, University
of New Mexico; Heath Garner and Katherine Mac¬
Donald of the Museum of Texas Tech University;
James Patton of the Museum of Vertebrate Zoology,
Berkeley; Mark Engstrom and Burton Lim of the Royal
Ontario Museum; Donald Wilson of the United States
National Museum of Natural History. We also thank
Robert Bull for assisting with laboratory work and two
anonymous reviewers for comments and suggestions
that greatly benefited the manuscript. Funding for this
project came from donations from James Sowell and
Alan Brown and from the Natural Science Research
Laboratory and Biological Database Initiative of Texas
Tech University.
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Addresses of authors:
Steven R. Hoofer
Department of Biological Sciences and
Natural Science Research Laboratory, Museum
Texas Tech University
Lubbock, TX 79409-3131 USA
Current address:
Department of Molecular Biosciences
The University of Kansas
Lawrence, KS 66045 USA
srhoofer@hotmail. com
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Phylogeny of phyllostomid bats (Mammalia:
Chiroptera): data from diverse morphological
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Sergio Solari
Department of Biological Sciences and
Natural Science Research Laboratory, Museum
Texas Tech University
Lubbock, TX 79409-3131 USA
Current address:
Instituto de Biologla
Universidad de Antioquia
Medellin, Colombia
ssolari@matematicas. udea. edu. co
14
Occasional Papers, Museum of Texas Tech University
Addresses of authors (cont.):
Peter A. Larsen
Department of Biological Sciences and
Natural Science Research Laboratory, Museum
Texas Tech University
Lubbock, TX 79409-3131 USA
peter. larsen@ttu. edu
Robert D. Bradley
Department of Biological Sciences and
Natural Science Research Laboratory, Museum
Texas Tech University
Lubbock, TX 79409-3131 USA
robert. bradley@ttu. edu
Robert J. Baker
Department of Biological Sciences and
Natural Science Research Laboratory, Museum
Texas Tech University
Lubbock, TX 79409-3131 USA
robert. baker@ttu. edu
Appendix
List of specimens examined, including geographic locality, tissue and voucher numbers, and GenBank
accession numbers for cytochrome-# and 16S rRNA sequences. Asterisks (*) by GenBank accession numbers
denote sequences generated in this study. Voucher specimens are housed in the following institutions: American
Museum of Natural History (AMNH); Carnegie Museum of Natural History (CM); Museo de Historia Natural,
Universidad Nacional Mayor de San Marcos, Peru (MUSM); Museum of Southwestern Biology, University of
New Mexico (MSB); Museum of Texas Tech University (TTU); Museum of Vertebrate Zoology, Berkeley (MVZ);
Royal Ontario Museum (ROM); and United States National Museum of Natural History (USNM). Museum
catalog numbers are missing for vouchers that are housed but not yet cataloged or the number is unknown.
Accession no.
Taxon Locality Tissue no. Voucher no. Cyt-b 16S
Artibeus amplus
VENEZUELA: Amazonas
VENEZUELA: Amazonas
A. concolor
SURINAME: Brokopondo
SURINAME: Brokopondo
SURINAME: Sipallawinie
A.fimbriatus
BRAZIL: Sao Paulo
PARAGUAY: San Pedro
PARAGUAY: Canindeyu
A. fraterculus
PERU: Lambayeque
ECUADOR: Guayas
ECUADOR: El Oro
ECUADOR: El Oro
A. hirsutus
MEXICO: Sonora
MEXICO: Michoacan
MEXICO: Michoacan
A. inopinatus
HONDURAS: Valle
HONDURAS: Valle
HONDURAS: Valle
HONDURAS: Valle
A. intermedins
COSTARICA: Guanacaste
HONDURAS: Copan
HONDURAS: Copan
A. jamaicensis
JAMAICA: St. Anns
ECUADOR: Loja
ECUADOR: Esmeraldas
ROM 107904
ROM 107847
TK 10378
TK 11240
TK 145271
TK 18991
TK 99588
TK 56670
TK 16631
TK 134686
TK 135408
TK 135760
NK 11128
TK 150585
TK 150598
TK 40184
TK 101201
TK 101202
TK 101203
TK 31924
TK 101993
TK 101996
TK 27682
TK 135290
TK 135905
ROM 107904
ROM 107847
CM 63792
CM 63789
TTU 104508
TTU 96431
TTU 94457
MVZ 168913
TTU 130519
TTU 102476
TTU 102814
MSB 54923
TTU 104509
TTU 104510
TTU 61115
TTU 83862
TTU 83863
TTU 83864
TTU 84650
TTU 84653
TTU 45295
TTU 103794
TTU 103109
AY642924 -
AY642923
U66518
U66519
FJ179223 FJ179173
U66498 -
DQ869391 -
DQ869390 -
U66499 -
DQ869389 FJ179174
DQ869388 FJ179175
FJ179224 FJ179176
U66500
FJ179225 FJ179180
FJ179226 FJ179181
U66501 -
FJ179227 FJ179177
FJ179228 FJ179178
FJ179229 FJ179179
U66502
FJ179230 FJ179182
FJ179231 FJ179183
DQ869480 FJ179187
FJ179232 FJ179186
- FJ179188
Hoofer et al.—mtDNA Phylogeny of Artibeine Bats
15
Appendix (cont.)
A. lituratus
A. obscurus
A. planirostris
A. schwartzi
Chiroderma villosum
C. saJvini
Dermanura anderseni
D. azteca
D. bogotensis
D. cinerea
D. glauca
D. gnoma
D. phaeotis
D. rava
D. rosenbergi
D. tolteca
D. watsoni
Ectophylla alba
Enchisthenes hartii
Uroderma magnirostrum
TRINIDAD & TOBAGO: Trinidad
TK 25029
ECUADOR: Pastaza
TK 104112
ECUADOR: Esmeraldas
TK 104525
ST. VINCENT AND THE GRENADINES:
Union Island
TK 128642
SURINAME: Nickerie
TK 17080
SURINAME: Para
TK 17308
FRENCH GUIANA: Sinnamaiy
TK 18787
GUYANA: N.W. District
TK 86531
FRENCH GUIANA: Sinnamary
AMNH 267998
FRENCH GUIANA: Sinnamary
AMNH 267999
VENEZUELA: Guarico
TK 15013
PERU: Madre de Dios
TK 16633
SURINAME: Nickerie
TK 17073
FRENCH GUIANA: Sinnamary
TK 18788
ECUADOR: Pastaza
TK 104410
FRENCH GUIANA: Remire-Montjoly
TK 143051
ST. VINCENT AND THE GRENADINES: St.
Vincent
TK 82839
ST. VINCENT AND THE GRENADINES: St.
Vincent
TK 82842
TRINIDAD & TOBAGO: Trinidad
TK 25052
PERU: Cusco
TK 70524
BOLIVIA: Pando
NK 14319
PERU: Madre de Dios
TK 16635
MEXICO: Morelos
TK 82897
MEXICO: Queretaro
TK 82898
MEXICO: Queretaro
TK 82901
VENEZUELA: Merida
TK 19379
VENEZUELA: Merida
TK 19380
VENEZUELA: Merida
TK 19381
FRENCH GUIANA: Sinnamary
TK 18790
PERU: Cusco
TK 16636
ECUADOR: Pastaza
TK 104136
ECUADOR: Tungurahua
TK 104203
FRENCH GUIANA: Sinnamary
TK 18789
ECUADOR: Pastaza
TK 104116
ECUADOR: Pastaza
TK 104117
NICARAGUA: Managua
TK 5411
MEXICO: Chiapas
TK 82894
MEXICO: Guerrero
TK 82895
MEXICO: Tabasco
TK 82896
HONDURAS: Atlantida
TK 136188
HONDURAS: Colon
TK 136234
ECUADOR: Esmeraldas
TK 104590
ECUADOR: Esmeraldas
TK 104592
ECUADOR: Guayas
TK 134526
ECUADOR: Guayas
TK 134611
ECUADOR: Esmeraldas
TK 104501
ECUADOR: Esmeraldas
TK 104509
ECUADOR: Esmeraldas
TK 135691
PANAMA: Darien
TK 22579
MEXICO: Chiapas
TK 82899
MEXICO: Morelos
TK 82900
HONDURAS: Comayagua
TK 136023
HONDURAS: Comayagua
TK 136035
MEXICO: Sinaloa
TK 4723
NICARAGUA: Zelaya
TK 7877
HONDURAS: Colon
TK 136988
COSTARICA: Limon
TK 16395
COSTARICA: Limon
TK 125311
PERU: Huanuco
TK 22690
PERU: Cusco
TK 55331
EL SALVADOR: San Miguel
TK 46006
TTU 84884
TTU 85297
TTU 104511
CM 68951
TTU 35725
AMNH 267210
AMNH 267998
AMNH 267999
TTU 33333
MVZ 170016
CM 68950
AMNH 267202
TTU 85182
CM 83901
CM 83210
CM 83218
CM 97374
MUSM 13611
MSB 57026
MVZ 166563
CM 78457
CM 78458
CM 78459
AMNH 267197
MVZ 173952
TTU 84908
TTU 84975
AMNH 267200
TTU 84888
TTU 84889
TTU 30513
TTU 103810
TTU 104100
TTU 85362
TTU 85364
TTU 103616
TTU 103701
TTU 85273
TTU 85281
TTU 103170
TTU 104294
TTU 104306
TTU 35568
TTU 30536
TTU 104077
ROM 108296
USNM 568512
CM 98710
USNM 582822
TTU 62670
U66505
FJ179233
DQ869393
FJ179234
U66506
U66507
FJ179235
DQ869424
U66508
U66503
U66504
DQ869410
DQ869398
DQ869524
DQ869525
DQ312414
U66509
FJ179236
FJ179237
FJ179238
FJ179239
FJ179240
DQ869386
U66511
U66512
FJ179241
FJ179242
U66513
FJ179243
FJ179244
U66514
FJ179245
FJ179246
FJ179247
DQ869387
FJ179248
FJ179249
FJ179250
FJ179251
FJ179252
FJ179253
FJ179254
U66515
FJ179255
FJ179256
FJ179257
FJ179258
U66510
U66516
FJ179259
AY157033
DQ312404
U66517
DQ312405
FJ179194
FJ179195
FJ179196
FJ179185
FJ179184
AF263225
AF263226
FJ179189
FJ179191
FJ179190
FJ179193
FJ179192
AY395837
FJ179198
FJ179197
FJ179199
FJ179200
FJ179201
FJ179202
FJ179203
FJ179204
FJ179222
FJ179206
FJ179207
FJ179208
FJ179209
FJ179218
FJ179217
FJ179212
FJ179210
FJ179211
FJ179220
FJ179221
FJ179219
FJ179213
FJ179215
FJ179214
FJ179216
FJ179205
AY395811
AY395838
AY395831
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