AMERICAN MUSEUM Novitates
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Number 3467, 24 pp., 8 figures, 10 tables December 30, 2004
Evolution of Caste in Neotropical Swarm-Founding Wasps (Hymenoptera: Vespidae; Epiponini)
FERNANDO B. NOLL,' JOHN W. WENZEL,” AND RONALDO ZUCCHI
ABSTRACT
Reproductive castes are compared in species of swarming wasps representing all currently
recognized genera of Epiponini (Polistinae). New morphometric data for nine measures of body parts and ovarian data are presented for 13 species. These are integrated with all similarly conducted available studies, giving a total of 30 species. Analysis reveals several syndromes relating reproductive and nonreproductive individuals: no meaningful distinction, physiological differences only, reproductives larger than nonreproductives with intermediate individuals pre- sent, reproductives different in shape from nonreproductives with no intermediates, and re- productives smaller in some aspects than nonreproductives. Distribution of these syndromes among species is consistent with phylogenetic relationships derived from other data. Optimiz- ing these syndromes on the cladogram indicates that the basal condition of Epiponini is a casteless society that is not comparable to the primitively social genus Polistes where dominant queens control reproduction. Castes originate several times in Epiponini, with different results in different lineages. The best documented evolutionary sequence passes from casteless so- cieties, to those with reproductives larger, to those with reproductives differing in shape from nonreproductives, to those with reproductives smaller in some measures. This sequence is consistent with Wheeler’s theory of the origin of caste through developmental switches, and represents the most thorough test of that theory to date.
INTRODUCTION In some species, reproductive “‘queens”’ and
es ale | nonreproductive “‘workers’’ differ only in Separation into castes is one of the cor- behavior, but in other species such behaviors nerstones of the evolution of social insects. are accompanied by physiological and mor-
' Departamento de Zoologia e Botanica; Instituto de Biociéncias, Letras e Ciéncias Exatas, UNESP; Rua Cristé6vao
Colombo, 2265; 15054-000, Sao José do Rio Preto, SP; Brazil (noll@dzb.ibilce.unesp.br).
? Department of Entomology, The Ohio State University, 1315 Kinnear Road, Columbus, OH 43212 (wenzel.
12 @osu.edu).
3 Departamento de Biologia, Faculdade de Filosofia Ciéncias e Letras de Ribeiraéo Preto, Universidade de Sao
Paulo, Brazil (rzucchi @ffclrp.usp.br).
Copyright © American Museum of Natural History 2004 ISSN 0003-0082
2 AMERICAN MUSEUM NOVITATES
phological specializations and body-size var- iation (Oster and Wilson, 1978). The degree to which castes are distinct often serves as part of the definition of the society itself, with greater caste differentiation indicating “higher”? sociality (Bourke, 1999). In some groups, such as swarm-founding neotropical wasps, the species are described as highly so- cial, although the distinction between queens and workers is considered slight and often confusing (Richards and Richards, 1951; Richards, 1978, cited as Polybiini, junior synonym of Epiponini, see Carpenter, 1993, £99%).
Wasps (Hymenoptera: Vespidae) have fre- quently been used to test evolutionary mod- els for the origin of social behavior because of their different levels of sociality—from solitary to eusocial (West-Eberhard, 1978, 1996; Wilson, 1985; It6, 1986; Spradbery, 1991). General theory holds that primitive systems of dominance rely on physical ag- gression, with the winner becoming the eg- glayer. More derived systems require some kind of caste determination that may occur during the immature stages of an individual’s development (preimaginal determination), with an unambiguous physiological or mor- phological result that cannot be reversed. Ab- sence of morphological castes is a plesiom- orphic (“‘primitive’’) condition in the three subfamilies of social wasps, so that morpho- logical castes were attained independently in different lineages (Carpenter, 1991). Most distant to the question at hand, females of Stenogastrinae are barely distinguished as queens or as workers (Turillazzi, 1991). Closer, and sister to the subfamily examined here, queens of Vespinae are larger than workers (Spradbery, 1991), but such a trait may be an adaptation for a queen’s solitary winter survival in most species (West-Eber- hard, 1978). In the Polistinae (studied here), the most basal genera (Polistes and Mischo- cyttarus), initiate their nests solitarily, with egglayers only slightly larger than non-eg- glayers. However, polistines present a large
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diversity that can be arranged along a spec- trum from taxa in which queens and workers are externally similar, to others with fairly distinct caste attributes (reviewed in O’Donnell, 1998; Shima et al., 1998). The Paleotropical tribe Ropalidini (perhaps the sister to the Neotropical tribe Epiponini ex- amined here) shows diversity that is hard to interpret without more study. For instance, some species of Ropalidia present distinct morphological castes (Yamane et al., 1983), including those of small colony size (Wenzel, 1992), but others show morphologically sim- ilar castes despite larger colony size (Gad- agkar and Joshi, 1982, 1983; Yamane and It6, 1987; Gadagkar, 1987). Parapolybia has castes (Yamane and Maeta, 1985) but their behavior is poorly known. Belonogaster is also poorly known (Pardi and Piccioh, 1981) but is thought to show great morphological variation (Keeping, 2000, 2002). In Poly- bioides, morphological castes are known in P. tabidus (Turillazzi et al., 1994), which builds large colonies and reproduces by swarms. However, despite the repeated evo- lution of castes in social wasps as a whole, the evolution of castes is largely interpreted through our understanding of Epiponini. Epiponini is a tribe of Polistinae, with about 20 well-marked genera and at least 229 species, plus another 27 subspecies, all of which are Neotropical. All Epiponini are po- lygynic (meaning that many queens com- monly reproduce simultaneously on the same nest), and all reproduce by swarms, which is taken as a sign of sophisticated, obligatory, high sociality. Initially, Richards (1978) doc- umented three forms of caste discrimination, and recent research builds upon these: (1) Queens larger than workers. In some species caste differences are so pronounced that they must be determined by nutritional differences during larval development (Evans and West- Eberhard, 1970; Jeanne and Fagen, 1974; Sakagami et al., 1996; Noll et al., 1997), with important consequences for fertility and re- productive asymmetries (West-Eberhard,
2004
1978; O’Donnell, 1998). The classical land- mark is a case of different, nonallometric castes of Agelaia areata, where queens and workers have different shapes as well as dif- ferent sizes (Jeanne and Fagen, 1974). It seems that these differences must represent preimaginal bias in nutrition. (2) Allometric differences, with queens smaller than work- ers in some body parts, but larger in others, which may result from ontogenetic repro- gramming in growth parameters (Jeanne et al., 1995), according to the idea that the body plans represent fundamentally different end products, not different points along a contin- uum. Sometimes such castes are barely de- tectable (Jeanne, 1996). (3) Slight or indis- tinct morphological differences, with castes absent, or manifested weakly, based on only a few traits (Richards, 1978; Jeanne, 1980). One great problem is that integration of the empirical studies is not straightforward be- cause few studies are exactly comparable in measurement methodology or phase of col- ony cycle studied, so generalization is diffi- cult. A rough summary of species known to fall into these three conditions can be found in table 1. It has been suggested that prei- maginal determination may be basal for Epi- ponini (Jeanne et al., 1995; Jeanne, 1996; Hunt et al., 1996; O’Donnell, 1998), espe- cially because such a trait is present in Apoi- ca (Shima et al., 1994), the most basal genus in Epiponini. However, Apoica is peculiar and highly apomorphic in many ways (gen- eral morphology, nest architecture, and noc- turnal habit, see Richards, 1978; Wenzel, 1992; and Pickett, 2003) and so it may not be a good model of basal synapomorphies of Epiponini. It has not been demonstrated that preimaginal determination is the basal con- dition for the whole clade.
Integrating studies of caste in Epiponini is difficult because studies to date have been limited in scope, with most publications cov- ering one species at a time. Measurements are not necessarily comparable across stud- ies. There are sometimes doubts about the
NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS
TABLE 1 Morphometric Differences Reported from Literature
No Significant Differences: Angiopolybia pallens!2.15, Asteloeca traili}2, Brachygas- tra lecheguana?5, B. moebiana}5, Chartergellus commu- nis'5.17, Clypearia sulcata!2, M. cingulata'3.'4, Parachar- tergus smithii8, Pa. colobopterus*6, Pa. fraternus'5.2}, Polybia bicytarella!3, Po. chrysothorax!s, Po. erythro- thorax!5, Po. micans!5, Po. quadricincta'!>, Synoeca cha- libea!s, S. surinama'2.!5, Pseudopolybia vespiceps*4
Queens Larger: Agelaia areata®, A. fulvofasciata!s, A. lobipleura's, A. yepocapa>, Brachygastra augusti3., B, bilineolata's, Charterginus fulvus!2, Chartergus chartarius!5, C. glo- biventris'0, C. metanotalis!2, Epipona tatua'2.|5, E. gue- rini4, Leipomeles dorsata'2, Metapolybia docilis?, Nectarinella championi'2, Polybia belemensis'5, Po. bistriata!3.», Po. catillifex'3.¢, Po. emaciata!s, Po. jurinei'5, Po. occidentalis'5.\9, Po. platycephala, Po. sylvestris'3, Po. rejecta\2.!5, Po. ruficeps'5, Po. scutellaris'5.\8, Po. singularis!5, Po. spinifex'2, Po. striata'5, Protonectarina sylveirae?3, Protopolybia exigua!0, Pr. minutissima}3, Pr. pumila'3, Pr. sedula's, Pseudopolybia compressa'5, Synoeca cyanea?
Queens Smaller in Some Measures, Larger in Others: Agelaia multipicta'!, Ag. pallipes's.'|, Ag. vicinal, Apoica flavissima?2, Ap. gelida's, Ap. pallens!5.16, Brachygastra scutellaris'3.\4, Metapolybia aztecoides'2, Polybia dimidiata's.20, Po. liliacea\!2, Pseudopolybia difficilis?
Index to References: a Richards (1978) found no differences. b Carpenter and Ross (1984) found queens slightly smaller than workers, but not significantly different.
c Richards and Richards (1951) found no differences. 1 Baio et al. (1998) 14 Carpenter and Ross 2 Baio et al. (2003a) (1984) 3 Baio et al. (2003b) 15 Richards (1978) 4 Hunt et al. (1996) 16 Jeanne et al. (1995) 5 Hunt et al. (2001) 17 Mateus et al. (1999) 6 Jeanne and Fagen 18 Noll and Zucchi (2000) (1974) 19 Noll et al. (2000) 7 Jeanne (1996) 20 Shima et al. (1996b) 8 Mateus et al. (1997) 21 Mateus et al. (2004) 9 Noda et al. (2003) 22 Shima et al. (1994) 10 Noll and Zucchi (2002) 23 Shima et al. (1996a) 11 Noll et al. (1997) 24 Shima et al. (1998) 12 Present data 25 Shima et al. (2000) 13 Richards and Richards 26 Strassmann et al. (1951) (1991)
- AMERICAN MUSEUM NOVITATES
phase of colony cycle that was measured, particularly when the colony was collected opportunistically by visitors on brief field- trips. In addition, when reproductive status does not relate closely to morphological var- iation, there is a tendency to rescue a concept of caste by categorizing problematic females as ‘‘laying workers’’ or ‘‘replacement queens”’ on an ad hoc basis. Such axiomatic descriptions may serve only to obscure the original question, protecting an inadequate concept of caste itself from refutation by em- pirical data. We address these issues by pre- senting here the most complete set of com- parable values regarding caste determination. A total of more than 13,500 measures en- compassing nine dimensions of 13 species are offered for the first time. These are in- tegrated with comparable data from other studies to include 68 species. We establish the basal condition for Epiponini, providing evidence for both preimaginal and postima- ginal caste determination. In addition to mor- phometric variation in caste, we stress the ex- istence of various types of social regulation.
MATERIALS AND METHODS
Workers and queens were taken from ma- ture colonies (i.e., post worker emergence) of 13 different species of Epiponini collected in three different localities. Angiopolybia pal- lens (Lepeletier), Asteloeca ujhelyii (Ducke), Charterginus fulvus Fox, Clypearia sulcata (de Saussure), and Leipomeles dorsata (Fa- bricius) were collected in Iquitos, Peru. Nec- tarinella championi (Dover) was collected in Costa Rica, near Atenas. For these two lo- calities, the samples were collected by John W. Wenzel and James Carpenter, killed in cy- anide and preserved promptly in 70% etha- nol, and deposited in the AMNH. Polybia (Polybia) liliacea (Fabricius), Polybia (For- micicola) rejecta (Fabricius), Chartergus me- tanotalis Richards, Epipona tatua (Cuvier), Metapolybia aztecoides Richards, Polybia (Pedothoeca) spinifex Richards, and Synoeca surinama (Linnaeus) were collected in Nova Xavantina, Mato Grosso, Brazil by Fernando B. Noll and Sidnei Mateus. Vouchers are de- posited at the Museu de Zoologia (MZUSP),
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Sao Paulo, Brazil, and the AMNH. They were taken by being put into a plastic bag provided with ether-moistened cotton balls or with open cyanide tubes. Populations were fixed in Dietrich’s solution and then kept in 70% ethanol for dissection.
From each of these colonies 100 workers and all queens were measured and dissected. When castes could be discriminated by size or color, all possible queens were selected, and from the remaining individuals 100 workers were arbitrarily selected. In small colonies where castes were not obvious, all individuals were measured and dissected. In large colonies where castes were hard to identify, 100 individuals were chosen ran- domly. After identifying some morphological characters to discriminate queens, such as ab- dominal size, all individuals having such a pattern were chosen and used in the analysis. The following characters were measured un- der a binocular microscope (smallest unit = 0.01 mm): head width (HW), minimum in- terorbital distance (IDm), gena width (GW), width of mesoscutum (MSW), alitrunk length (AL), length of gastral tergite I (T,L), basal height of T, (T,BH), basal widths of tergite II (T,BW), and partial length of the forewing (WL) (fig. 1, for more details about the characters see Shima et al., 1994). Ovary condition was determined under a stereomi- croscope. In order to analyze insemination, the spermatheca was removed and put on a slide in a 1:1 solution of glycerin and ethanol (70%). The presence of sperm cells was con- firmed by microscope.
Before statistical analysis, data were con- verted to millimeters and later converted by log transformation in order to avoid prob- lems of variance. Means and standard devi- ations were calculated from the nine mor- phological measurements. Statistical charac- terization of caste was explored in two ways. One-way ANOVA was used for comparisons of means to demonstrate whether castes (as determined by dissection) differ in some body dimensions. Because multiple measures that relate to shape are not always captured well in single comparisons, stepwise discrim- inant function analysis was used to see if combinations of variables could be useful in predicting caste. In this method, variables are successively added to the model based on the
2004
NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 2
Fig. 1.
Representative measures for morphometric analyses of this paper: head width (HW), mini-
mum interorbital distance (IDm), gena width (GW), width of mesoscutum (MSW), alitrunk length (AL), length of gastral tergite I (T,L), basal height of T, (T,BH), basal widths of tergite I] (T,BW), and partial
length of the forewing (WL).
higher F to enter values, adding no more var- iables when the F-ratio is no longer signifi- cant. However, variables that enter the model early may be completely subsumed by sep- arate variables that enter later. The signifi- cance of Wilks’ lambda (an estimate of com- mon variance between sets of variates) was used to determine the degree to which sep- arate measures contributed to the final model. This is an alternative to using an F to remove at each step. Variables that appear in the final model but do not have significant F-ratios represent variance components that are ex- plained by some combination of the other variables also in the model, and therefore no longer contribute to the discrimination itself. Wilks’ lambda varies from zero to one: the lower the value, the greater the significance.
Analysis of covariance (ANCOVA) was used, with alitrunk length (AL) as a covari- ate, in order to identify different growth rates in the body parts measured. AL was chosen
based on the effectiveness in previous pub- lications (Jeanne et al., 1995; Jeanne, 1996; Hunt et al., 1996).
RESULTS OVARIAN DEVELOPMENT
The ovariole number was always three in each ovary, and the following types of ovar- ian development were distinguished (table 2); type A: with filamentous ovarioles that had no visible oocytes or with some very small oocytes; type B: bearing some young oocytes; type C: with one or more mature oocytes in each ovariole; type D: with well- developed and very long ovarioles coiled in- side the gaster, with at least one mature egg. Only females with type D ovaries were in- seminated. All four types were found in the following species: Angiopolybia pallens, Charterginus fulvus, Leipomeles dorsata, and Nectarinella championi (table 2). Type
6 AMERICAN MUSEUM NOVITATES
TABLE 2 Ovary Development for All Species Analyzed?
N Ovaries (%)
females A B Cc D Angiopolybia pallens 50021 7 54 28 Asteloeca ujhelyii 18 22 28 50 Charterginus fulvus 29 79.3 20.7 Chartergus metanotalis 812 = 67 24 9 Clypearia sulcata 138 73.6 25 1.4 Epipona tatua 6,752 66.5 33 0.5 Leipomeles dorsata 10541 Bi. She m2 Metapolybia aztecoides 251 59 27 14 Nectarinella championi 98 «4 21 29 =~ Ii Polybia liliacea 22,384 66.6 33 0.4 Polybia rejecta 3,838 60 38 2 Polybia spinifex 997 43.9 55 1.1 Synoeca surinama 1478 48 45 7
aSee text for explanation.
C was not found in Asteloeca ujhelyii, Char- tergus metanotalis, Occipitalia sulcata, Epi- pona tatua, Metapolybia aztecoides, Polybia liliacea, Polybia rejecta, Polybia_ spinifex, and Synoeca surinama (table 2). Queens’ Ova- ries (type D, inseminated) were much longer than workers’ ovaries in Chartergus metano- talis, Epipona tatua, Polybia liliacea, Polybia rejecta, and Polybia spinifex. No species of this study lacked both types B and C.
MORPHOLOGICAL DIFFERENCES
Differences of mean values of nine char- acters measured were tested in workers and
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queens (tables 3—6). Univariate statistics (ANOVA) showed that measured characters could be different or not between queens and workers in different species. Also, based on multivariate statistics, the power of discrim- ination of each measurement varied in the different species studied; that is, the mea- surements may discriminate castes indepen- dently or only in combination.
In a first group (fig. 2), morphological dif- ferences between castes were totally or prac- tically absent in the following species: An- giopolybia pallens, Asteloeca ujhelyii, Cly- pearia sulcata (table 3), Leipomeles dorsata, Metapolybia aztecoides, Nectarinella cham- pioni, and Synoeca surinama (table 4). AN- OVA showed no significant differences in any measurement in An. pallens, As. ujhelyit, and Cl. sulcata; in S. surinama, only one measurement was significant, and in L. dor- sata, M. aztecoides, and N. championi three measurements were significant. Except for M. aztecoides, in which some characters were smaller in queens than in workers, dif- ferences were always based on queens being larger than workers. ANCOVA, using ali- trunk length as a dependent variable (table 7), was not significant in any character in An. pallens, As. ujhelyii, and Cl. sulcata. In L. dorsata, M. aztecoides, N. championi, and S. surinama, significant differences were de- tected.
Wilks’ lambda values were used to infer the independent contribution of each variable
TABLE 3
Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of Angiopolybia pallens, Asteloeca ujhelyii, and Clypearia sulcata
Angiopolybia pallens Asteloeca ujhelyii Clypearia sulcata
Queens Workers ANOVA Queens Workers ANOVA Queens Workers ANOVA
(N = 18) (N = 82) (F) (N = 9) (N = 9) (F) (N = 10) (N = 115) (F) HW 449+0.05 444+0.45 0.28 3.34+0.07 3.35+0.10 0.01 3.06+ 0.03 3.02+0.07 0.75 IDm 0.77+0.06 0.76+0.06 0.40 163+0.05 163+0.05 0.01 1.25+0.03 1.25+0.03 0.03 GW 1.87+0.03 1.86+0.04 0.19 0.98+0.05 0.97+0.07 0.01 0.53 +0.03 0.53+0.02 1.93 MSW 2.82+0.06 2.82+0.07 0.01 1.99+0.09 2.07+0.15 2.05 1.86+0.03 2.00+0.18 1.12 AL 6.02+0.15 5.97+0.18 1.22 4.59+0.21 452+0.18 2.08 4.27+0.12 4.00+0.20 3.79 T,L 3.654014 3.654019 0.01 2.5640.10 2.51+011 2.91 2.284015 2.15+0.13 1.87 T,BH 0.67+0.03 0.68+0.04 0.67 0.51+0.03 0.49+0.05 0.83 0.32+0.01 0.34+0.04 0.30 T,BW 169+0.07 1.70+0.07 0.04 0.95+0.06 0.99+0.10 0.93 1.13+0.02 1.22+0.15 0.76 WL 6.65+0.14 664+0.12 0.14 4.64+041 4.774018 0.72 3.34+0.08 3.30+0.12 0.16
No differences are significant at p < 0.05.
2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS i TABLE 4 Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of Leipomeles dorsata, Metapolybia aztecoides, Nectarinella championi, and Synoeca surinama Leipomeles dorsata Metapolybia aztecoides Queens Workers ANOVA Queens Workers ANOVA (N = 13) (N = 92) (F) (N = 35) (N = 216) (F) HW 2.04 + 0.03 2.01 + 0.03 LAST * 1.67 + 0.06 1.66 + 0.07 0.05 IDm 0.72 + 0.02 0.72 + 0.02 0.30 1.09 + 0.04 1.09 + 0.06 0.001 GW 0.40 + 0.02 0.40 + 0.03 0.01 0.71 + 0.03 0.72 + 0.04 0.003 MSW 2.09 + 0.10 2.06 + 0.11 0.80 0.94 + 0.04 0.96 + 0.04 LOSE AL 1.19 + 0,03 1.17 + 0.03 4.69* 2.08 + 0.09 2.09 + 0.11 0.33 T,L 1.36 + 0.05 1.31 + 0.09 2.50 1.47 + 0.08 1.49 + 0.08 2.43 T,BH 0.21 + 0.03 0.21 + 0.02 0.01 0.30 + 0.02 0.31 + 0.03 4,.21* T,BW 0.79 + 0.04 0.77 + 0.04 1.19 1.32 + 0.07 1.28 + 0.07 12.82*** WL 2.38 + 0.07 2.31 + 0.09 4.97* 2.07 + 0.08 2.04 + 0.08 3.55 Nectarinella championi Synoeca surinama Queens Workers ANOVA Queens Workers ANOVA (N = 13) (N = 92) (F) (N = 26) (N = 187) (F) HW 2.13 + 0.03 2.10 + 0.027 FQS** 3.88 + 0.08 3.86 + 0.10 0.53 IDm 0.92 + 0.03 0.91 + 0.022 0.51 1.86 + 0.05 1.85 + 0.05 0.94 GW 0.56 + 0.05 0.57 + 0.03 0.17 0.99 + 0.07 0.96 + 0.07 4.54*** MSW 1.61 + 0.04 1.58 + 0.05 1.9] 6.03 + 0.14 5.92 + 0.43 1.56 AL 2.33+ 0.11 2.29 + 0.071 2.04 2.74 + 0.07 2.72 + 0.09 2.08 T,L 1.37+0.11 1.26 + 0.07 12.02*** 3.58 + 0.14 3.56 + 0.12 1.06 T,BH 0.24 + 0.02 0.25 + 0.028 1.35 1.18 + 0.05 1.18 + 0.06 0.36 T,BW 1.33 + 0.06 1.23 + 0.151 4.40* 1.77 + 0.07 1.75 + 0.07 1.75 WL 2.29 + 0.05 2.31 + 0.07 1.60 6.68 + 0.12 6.64 + 0.18 1.00 *#%D < 0.001; **p < 0.02; *p < 0.05. TABLE 5 Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of Charterginus fulvus, Chartergus metanotalis, and Epipona tatua Charterginus fulvus Chartergus metanotalis Epipona tatua Queens Workers ANOVA Queens Workers ANOVA Queens Workers ANOVA (N = 6) (N = 22) (F) (N = 9) (N = 45) (F) (N = 46) (N = 54) (F) HW 4.49+0.04 443+0.05 7.82** 5.64 +0.07 5.65+0.07 0.30 3.79 + 0.06 3.69+0.07 60.3*** IDm 160+0.06 1.56+0.04 2.99 2.34+0.05 2.28+0.05 20.75*** 1.73+0.04 1.68+0.05 35.2*** GW 0.43 + 0.02 0.40+0.03 4.53** 0.72+0.13 0.74+0.05 9.87*** 0.94+0.05 0.88+0.06 28.7*** MSW 3.38+0.06 3.28+0.07 8.39** 440+0.11 4.31+0.08 42.8*** 2.68 + 0.08 2.55+0.08 80.7*** AL 5.75+0.16 5.66+0.16 1.70 7402£0.20 7.(0520:18 11.27*** 7.432019 7.034£0.25 79.1*** T,L 4.35+0.16 4.094013 17.17*** 5.:12+0.15 5.01+0.23 1.67 ser tOl§ 3.052017 33.1*** T,BH 0.63 +0.03 0.61+0.03 1.50 0.62+0.05 0.61+0.04 0.50 0.64+0.03 0.61+0.03 27.4*** T,BW 3.63+0.05 3.50+0.12 7.60** 5.85+0.10 5.83+0.11 37.47*** 1.33+0.04 1.27+0.06 33.1*** WL 5.24+0.10 5.14+0.11 4.30* 9.40+0.16 9.00+0.30 0.30 4.42+0.09 4.24+0.13 62.9***
***D < 0.001; **p < 0.02; *p < 0.05.
8 AMERICAN MUSEUM NOVITATES NO. 3467
TABLE 6 Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of Polybia liliacea, Polybia rejecta, and Polybia spinifex
Polybia liliacea Polybia rejecta Polybia spinifex
Queens Workers ANOVA Queens Workers ANOVA Queens Workers ANOVA
(N = 84) (N = 66) (F) (N = 21) (N=79) (F) (N= 11) (N = 100) (F) HW 3.68+0.06 3.81 +0.03 200.6*** 2.99+0.03 2.95+0.05 21.87*** 5$66+0.04 5.44+0.13 32.8*** IDm 167+0.05 1.62+0.05 45.7*** 1.24+0.03 1.16+0.03 89.9*** 2.79 +0.07 2.65+0.09 23.11*** GW 0.70+0.05 0.62+0.03 167.9*** 0.50+0.04 0.48 + 0.04 5.14% 1.01 +0.04 1.01+0.10 0.01 MSW 2.84+0.08 2.6140.05 418.5*** 2.274005 2.14+0.07 63.4*** 3.78 + 0.04 3.43+0.14 75.95*** AL 6.10+0.14 5.874012 112.8*** 4704008 4384011 147.01*** 8314010 7.70+0.32 40.22*** T,L 3.16+0.36 2.91+0.10 29.7*** 261+0.09 2.42+0.10 65.4*** 5.42+0.15 499+0.24 33.91*** T,BH 0.69+0.04 0.60+0.04 208.7*** 0.45+0.03 041+0.02 25.01*** 0.86+0.04 0.79+0.06 15.79*** T,BW 2.36+0.11 2.07+0.06 380.3*** 1.37+0.07 1.2340.08 58.49*** 2.3440.07 2.02+0.13 66.74*** WL 5.13+0.08 5.07+0.10 14.8*** 3.8840.08 3.734010 44.33*** 9404016 9.00+0.30 18.75***
** < 0.001; **p < 0.02; *p < 0.05.
to the model that predicts the caste of the individual wasps. Significance values of the loadings of each morphometric variable in- dicate whether that variable contributes meaningfully to the prediction of caste. Anal- ysis showed that, in the above species, Wilks’ lambda values were always high, ranging from 0.7 to 1.0 (table 8). Consider- ing that lambda is defined as 1.0 minus the squared canonical correlation, the highest value is 1.0, indicating complete absence of association. These data indicate that morpho- logical castes are practically absent in these species, based on these measures. Specifical- ly, even if queens may differ from workers on average, the ability to identify an individ- ual as a queen or worker based on morpho- metric values is very poor. None of the queens were correctly classified by discrim- inant scores in An. pallens or Cl. sulcata, and relatively few in L. dorsata, M. aztecoides, N. championi, and S. surinama (see table 10). Only in As. ujhelyii are castes better discrim- inated.
In a second group (fig. 3)—Charterginus fulvus, Chartergus metanotalis, Epipona ta- tua, Polybia rejecta, and P. spinifex—queens were larger than workers. Mean differences using ANOVA (tables 5, 6) were found in five of nine characters in Cn. fulvus and Cg. metanotalis. In E. tatua, Po. rejecta, and Po. spinifex all body measurements were differ- ent.
Multivariate analysis showed that the mea-
surements had a low power of discrimination in Cn. fulvus, Cg. metanotalis, and E. tatua (tables 8, 9), and that discrimination between castes can only occur based on a combination of measurements. In Polybia rejecta and Po. spinifex, differences were much more pro- nounced and all measurements were stronger discriminators. Wilks’ lambda ranged from 0.1 to 0.3 (table 9), and castes were more clearly discriminated than in the previous group (table 10). ANCOVA showed signifi- cant differences in growth rates of body parts in at least one character in all species of this group (table 7).
In a third class, Polybia liliacea castes were as clearly distinct as in the second group, but head width was smaller in queens than in workers (table 6). ANOVA showed that all measurements were different between queens and workers.
DISCUSSION
A distinct physiological separation of fe- males into those that are reproductive and those that are nonreproductive is possible based on ovarian condition and insemination in some of the species reported here. While complete absence of ovarian development in workers (i.e., the absence of both types B and C) was not found in the species studied here, such a syndrome has been reported in Apoica flavissima, Agelaia vicina (Sakagami et al., 1996), Ag. pallipes, and Ag. multipicta (Noll
2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 9 1.6 3.05 4.5 7 Metapolybia aztecoides ¢ .» (Angiopolybia pallens . Clypearia Seog 1.5 2.95 0 bd 43) vf i e e oee¢ e 14 e poo 2.00 : r : fel ® *~ A hg peo peo A . pee a 44 ° @ ee S se at cal: ete) akg a Le of ta - i A5|) eee ae } 2 13 eo oA fae a 2 . o ; Meee q JP ae o* SIT T eiaanc ae eid ee oie ® . =e? oo°¢e @ = 220 ee e€ oO e e t H em © ieee ou o.° > @ eo @ een 39 i e © 12 eet oo eoe asf Oe" O o e e ° e. a" @ @ @ ry e o o e ; bd 2.70 1 S bd bd e i. e ® 3 e : ® 2.65 e e ®e 1.0 260 3.5 1.75 1.85, 1.99 2.05 2.18 225 1474 1.78 1.82 1.86 1.90 1.94 1.98 09 1.0 1 1.2 133 14 1.5 T2BW Dm T2BW 44 0.94 220 e Synoeca surinama | ee P y >» | -elpomeles dor Sade *® | Nectarinella championi 2.16 e 0.86 a : ; - oa ~ Fe o ® “ OF yO ow. Neer a 38 e oO oO - eee Waar > One Grek eer 22 - Oe ee en ae & ; o0 alae z ov aa a ig : .. 2 078 openved T 210 a We By O-@@0 e ea 36 e e o e e e eee a eo. “ & Veber e e d Oo a] e e -@ ee ae 208 074 _‘ e e 4 e e ~*@ oO, oO Sig © y 32 e fy te 204 : 0.66 2.02 ae Tig fis 15S iis es Tale 1.90 1.94 1.98 2.02 2.06 2.10 2.14 1.05 1.18 1.25 1.35 1.45 1.55 1.65 Tat: GW TiL 2.9 Asteloeca ujhelyii 28 oO 27 i ) DN e oO = 26 ‘ o 25 ° ae t- u se, se “a 24 e e oS e 2.3 0.42 0.46 0.50 0.54 0.58 0.62 T1BH Fig. 2. Slight caste discrimination found in some epiponines based mostly on shape (when appli-
cable). Individuals identified by dissection to be ‘‘queens”’ are represented as squares, while those identified as ‘“‘workers’”’ are solid dots. Separate regression lines are drawn for illustration only; see text
for discussion.
et al., 1997). In our present study, queens’ ovaries (type D) were much longer than workers’ ovaries in Chartergus metanotalis, Epipona tatua, Polybia liliacea, Po. rejecta, and Po. spinifex. This situation is also known in Apoica flavissima (Shima et al., 1994), Protonectarina sylveirae (Shima et al., 1996a), Polybia dimidiata (Shima et al., 1996b), Po. scutellaris, Po. paulista and Po. occidentalis (Noll and Zucchi, 2000), Age- laia vicina (Sakagami et al., 1996), and Ag.
pallipes and Ag. multipicta (Noll et al., 1997). Similarly, though less discrete, inter- mediate type C was not found in Asteloeca ujhelyii, Chartergus metanotalis, Clypearia sulcata, Epipona tatua, Metapolybia aztecoi- des, Polybia liliacea, Po. rejecta, Po. spini- fex, and Synoeca surinama (table 2). Other species previously reported to have similar distinction are Protonectarina sylveirae (Shi- ma et al., 1996a), Polybia dimidiata (Shima et al., 1996b), Po. scutellaris and Po. paulis-
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2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 11 a7 1.30 4 oO Ady Bae . } po oO Epipona tatua o Polybia liliacea 128 Polybia rejcta oe 35 Oo won oo ao o-o o oo ie 1.22 ee 33 oa ie ee Tat ee oooada eeeweoens pS Ae Stell Ye ence eo a eae Oo ie ont = e @eeoe oo e 1.18 Pe et s eoe ot 4 ef ie 34 ee Oot OO OD ” © eeTD @ e@ eee -@eeodn Oo “@ fia bo ee e -@eeenop aoa . “Me ue -—"@@ oeoee ee *, ° e ® e 110 e e ao ‘ ee ee8 e e e 27 = 5 - . 1.06 2.36 2.45 2.55 2.65 2.75 2.85 3.45 3.55 3.65 3.75: 3.85 3.95 1.95 2.00 2.05 2.10 2.15 2.20 2.30 2.35 2.40 MSW HW MSW 26 58 r r . x 458 . r . Polybia spinifex Chartergus piptagtals E Charterginus fulvus ai o 454 Al oo” ¥ o ao Oo : a eee a qo a Nesiig Aer eee ee ee Pd aes e oa oes eee ou if 22 5 e ee e wo e he aa 5.4 o oO oo $ in 5 ea c=. ee ee” 0 @ @ a Tat, oD See 42 pe tet. et See ‘oS, -@ @ eee oe. EO en hoc, he“ @ @ sof ae we ee : e 4 e e 4.34 e a ° 16 48 . . 430 . . . 31 3.2 3.3 a4 3.5 3.6 37 38 39 64 66 6.8 7.0 7.2 74 76 78 8.0 37 38 3.9 40 44 42 44 45 46 MSW AL TIL Fig. 3. Caste discrimination found in some epiponines based on size and shape. Individuals identified
by dissection to be “‘queens” are represented as squares, while those identified as “‘workers”’ are solid dots. Separate regression lines are drawn for illustration only; see text for discussion.
TABLE 9
Wilks’ Lambda and F-Statistics Lambda values estimate the degree of contribution for each separate measure to the final discriminant function model. In these cases values were about 0.5 and lower, indicating better discrimination if compared to those found in table 8. F-statistics for ANOVA using the same variables are shown, with appropriate
significance values.
HW GW IDm MSW AL TL T,BH T,BW WL
Chartergus Epipona Polybia Polybia Polybia metanotalis tatua liliacea rejecta spinifex Wilks’ A F Wilks’ A F Wilks’ F Wilks’ A F Wilks’ X F 0.44 5.54* 0.21 34.78*** 0.29 2.64 0.483 1.37 0.35 22.14*** 0.492 3.34 0.41 1.81 0.457 4,15* 0.17 1.53 0.30 4.76* 0.495 3.17 0.44 5.12* 0.463 5.46** 0.39 37.27*** 0.537. 13.15*** 0.48 10.78** 0.446 1.72 0.19 10.88*** 0.42 2.56 0.461 4.98* 0.18 8.82*** 0.46 8.16** 0.18 5.47** 0.32 11.43*** 0.539 = 13.64*** 0.41 2.27 0.447 1.96 0.492 3.53
***D < 0.001; **p < 0.02; *p < 0.05.
12 AMERICAN MUSEUM NOVITATES
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TABLE 10 Classification Scores for Group Comparisons Using Discriminant Analysis
Predicted classification
Observed Species classification Worker Queen % Correct Angiopolybia pallens Worker 82 0 100.0 Queen 18 0 0 Asteloeca ujhelyii Worker 7 2 77.8 Queen 1 8 88.9 Charterginus fulvus Worker 22 ] 95.7 Queen 1 5 83.3 Clypearia sulcata Worker 0 34 100 Queen 0 z 0 Epipona tatua Worker 45 9 83.3 Queen 5 41 89.1 Leipomeles dorsata Worker 4 19 82.6 Queen 4 9 69.2 Metapolybia aztecoides Worker 208 8 96.3 Queen 23 12 34.3 Nectarinella championi Worker 3 19 86.4 Queen 5 5 50 Polybia liliacea Worker 66 0 100 Queen 2 42 95.5 Polybia rejecta Worker 77 Z 97.5 Queen 1 20 95.2 Polybia spinifex Worker 98 2 98 Queen 0 11 100 Synoeca surinama Worker 186 1 99.5 Queen 4 9 69.2 Chartergus metanotalis Worker 6 40 87 Queen 6 62 91.2
ta (Noll and Zucchi, 2000), and Chartergus globiventris (Noll and Zucchi, 2002). Some species are found to have individuals repre- senting all four stages, implying a near con- tinuum (but that insemination is always as- sociated with type D ovaries). These species include Angiopolybia pallens, Charterginus fulvus, Leipomeles dorsata, and Nectarinella championi (table 2). The same pattern, im- plying a lack of physiological caste in any meaningful way, was previously found in other species using the same procedure, such as Chartergellus communis (Mateus et al., 1999), Pseudopolybia vespiceps (Shima et al., 1998), Parachartergus smithii (Mateus et al., 1997), and Brachygastra lecheguana (Shima et al., 2000).
Ovarian development presents a confusing array of conditions, yet previous researchers have tried to find ways to capture the totality of this variation with some kind of overarch- ing hypothesis of caste that would be applied to all species of Epiponini equally. For ex- ample, the concept of cyclical oligogyny in- vokes demography to provide a process by which individuals may become queens at swarm initiation of colonies, but not later in the colony cycle (West Eberhard, 1978). Col- ony cycle is known to relate to the degree of morphological differentiation in species that do have marked differences, with differences growing as colonies age (e.g., Noll and Zuc- chi, 2000, 2002), and comparing mature col- onies is now required if one is to argue that
2004
the animals that are sampled actually repre- sent the species’ breadth of morphological diversity. Nonetheless, the search for a single explanation of caste (its presence or its am- biguity) in Epiponini is still lacking. We offer here a novel view that relies on returning to the fundamental question of whether caste exists at all. We then integrate the answers to those questions to provide the most co- herent view of caste to date, one that does not seek to explain all Epiponini through a single fundamental process.
MORPHOMETRIC DIFFERENCES BETWEEN CASTES
Size divergence is usually regarded as an initial step for the origin of morphological castes in the three main groups of social Hy- menoptera (ants, bees, and wasps; Wheeler, 1991). In wasps, caste-related size differenc- es are conspicuous in the Vespinae, but com- plex in the Polistinae (fig. 4). However, the practice of comparing ratios of linear body measures (fig. 4) may be overly simple to capture the actual patterns of caste determi- nation. For this reason, we used not only lin- ear measures themselves, but also analysis of their covariance to look for shape differences associated with reproductive status as well as size differences.
In general, morphometric differences asso- ciated with ovarian status were either slight or absent in Angiopolybia pallens, Asteloeca ujhelyii, Clypearia sulcata (table 3), Leipo- meles dorsata, Metapolybia aztecoides, Nec- tarinella championi, and Synoeca surinama (table 4). Other studies found the same for Parachartergus smithii (Mateus et al., 1997), Pa. colobopterus (Strassmann et al., 1991), Pseudopolybia vespiceps (Shima et al., 1998), Chartergellus communis (Mateus et al., 1999), Brachygastra lecheguana (Shima et al., 2000), Synoeca cyanea (Noda et al., 2003), and Metapolybia docilis (Baio et al., 2003a). In this group, we might say that while some individuals are reproductive and some are not, there is no meaningful morphological caste. In some cases, caste appears to be what Kukuk (1994) called behaviorally eusocially determined in the adult stage. In Metapolybia and Synoeca (West-Eberhard, 1978, 1981), caste is apparently determined by disputes
NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 13
among adults rather than by larval manipu- lation. Young females have their ovaries sup- pressed in queen-right colonies, so that only through orphanage do young females develop their ovaries and become queens (West-Eber- hard, 1978). In such species, caste as a phys- iological state may be distinct even if it is impossible to recognize morphologically. Of particular interest may be Astleoca ujhelyii. In table 10 there is fairly good discrimination of reproductive “‘queens’’ and nonreproductive ‘“‘workers”’, with from 10 or 20% error. Table 8 shows that two values contribute signifi- cantly to the discriminant function model, meaning that the computer can find a way to separate reproductives and nonreproductives if they are labeled prior to analysis. However, table 3 shows that none of the linear metrics are significantly different between castes (see also fig. 2 for graphic representation of over- lap). Thus, this species presents a kind of in- termediate state in which reproductive status can be explained by shape differences after the fact, but not predicted based on the nine morphometric variables independently, in- cluding variables that are adequate to capture caste in other species (see below). Asteloeca ujhelyii occupies a region of parameter space that represents a shift between species with distinct reproductive castes and those that are casteless morphologically.
Species of Epiponini appear to represent a continuum from those without morphological castes (above) to those with discrete castes (below). There are now enough data to dem- onstrate this by presenting measures from species analyzed by the same _ protocols, whether in the present study or in the liter- ature. Plotting the percentage of queens cor- rectly classified by discriminant function analysis (table 10, and literature) versus Wilks’ lambda values (table 8 and 9, and lit- erature), we see that in many species queens are classified correctly from 80 to 100% of the time, while in other species classification is less effective (fig. 5). Breaking the contin- uum of figure 5 into logical parts, we find that species with low Wilks’ lambda for mor- phometric variables (1.e., they show strong covariance between morphometric measures and ovarian status) can be classified correctly most of the time (fig. 5, region A). Distinc- tions between reproductive and nonreproduc-
14 AMERICAN MUSEUM NOVITATES
NO. 3467
1.29
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0.88 0.98 1.08 1.18
Q/W ratio for WL
Fig. 4. Comparison of the level of caste distinction between epiponines (1-59, white circles indicate workers with ovarian development, black diamonds indicate workers without ovarian development) and a Vespinae (60, black square) based on wing length queen—worker ratio versus length of tergite I (except 14, 16, 17, 33-35, 37: hamuli number and 56: width of tergite I). 1. Agelaia areata, 2. A. fulvofasciata, 3. A. lobipleura, 4. A. multipicta, 5. A. pallipes, 6. A. vicina, 7. A. yepocapa, 8. Angiopolybia pallens, 9. Apoica flavissima, 10. A. gelida, 11. A. pallens, 12. Asteloeca ujhelyii, 13. Brachygastra augusti, 14. B. bilineolata, 15. B. lecheguana, 16. B. moebiana, 17. B. scutellaris, 18. Chartergellus communis, 19. Charterginus fulvus, 20. Chartergus chartarius, 21. C. globiventris, 22. C. metanotalis, 23. Clypearia sulcata, 24. Epipona tatua, 25. E. guerini, 26. Leipomeles dorsata, 27. Metapolybia aztecoides, 28. M. docilis, 29. Nectarinella championi, 30. Parachartergus colobopterus, 31. Pa. fraternus, 32. P. smithii, 33. Polybia bicytarella, 34. Po. bistriata, 35. Po. catillifex, 36. Po. dimidiata, 37. Po. emaciata, 38. Po. erythrothorax, 39. Po. jurinei, 40. P. liliacea, 41. P. occidentalis, 42. P. parvulina, 43. P. platycepha sylvestris, 44. P. quadricincta, 45. Po. rejecta, 46. Po. ruficeps, 47. Po. scutellaris, 48. Po. singularis, 49. Po. spinifex, 50. Po. striata, 51. Protonectarina sylveirae, 52. Protopolybia exigua, 53. Pr. minu- tissima, 54. Pr. pumilla, 55. Pr. sedula, 56. Pseudopolybia difficilis, 57. Ps. vespiceps, 58. Synoeca cyanea, 59. S. surinama, 60. Vespula squamosa. For references for the species, see table 1.
1.28
1.38
tive females may represent a general increase in all measures (e.g., Polybia rejecta or Po. spinifex, fig. 3, table 5) or in some measures more than others such that there is a con- spicuous shape difference as well (dramati- cally in Polybia liliacea, where queens are larger in all ways, except with smaller heads in absolute terms, fig. 3, table 6). In the mid-
dle of the continuum (fig. 5, region B) are species such as Asteloeca ujhelyii with high Wilks’ lambdas (weak covariance between measures and ovarian status). These may be without conspicuous size differences (fig. 2, table 3; fig. 5, region B; Asteloeca ujhelyii), but shape differences are enough to permit effective classification of reproductives
2004
100 é j Q ee Chartergus globiventris
(oe) ©
e)) oO
40
20
Queens correctly classified (%)
0 0.1 0.3
ock® Epipona tatua
NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 15
4S @ 3% A a Polybia spinifex x?
O \)? e® pe Ba Asteloeca ujhelyii & vO
& Brachygastra augusti G
© . aN Synoeca surinama
O Parachartergus smithii O
Caalerolnus fulvus
Leipomeles dorsata
O Chartergellus communis
Parachartergus fraternus Clypearia sulcata
O O Nectarinella championi C
O Metapolybia aztecoides Brachygastra lechequana
e) Pseudopolybia vespiceps O
Angiopolybia pallens o
0.5 0.7 0.9
Wilk's lambda
Figs.
Plots of Wilks’ lambda values versus queens correctly classified using discriminant function
analysis for some epiponines. See text for discussion.
nonetheless. These species that can be cor- rectly classified as queens or workers (fig. 5, regions A and B) show that there is no gen- eral rule for identifying reproductives, be- cause the way queens differ in shape from workers varies between species (tables 8, 9). Finally, in some species reproductives do not differ substantially in size or shape (e.g., An- giopolybia pallens, table 3, Nectarinella championi, table 4; fig. 2 and table 8; fig. 5, region C).
SHAPE: It has long been known that repro- ductive status in Epiponini is not strongly as- sociated with body size for many species. In- deed, the claim that morphological castes had arisen without a primordial size component was first made for social wasps (Jeanne et al., 1995). Castes in Apoica pallens differed significantly in body proportions but not in overall size. Such a finding indicates that morphological castes may not have their or- igins in a single allometric growth function along a body size gradient (Jeanne et al., 1995). It seems that in Apoica pallens, as
well as in several other epiponines (see be- low), the nature of queen—worker differences would be determined during the larval stage such that queen-destined larvae show differ- ent growth rates of various compartments compared to worker-destined larvae, gener- ating animals of different shape even though they are about the same size. In several spe- cies, not only shape but also size is involved, perhaps as a secondary acquisition (Jeanne, 1996: Hunt et al. 1996).
Hunt et al. (1996) proposed that shape dif- ferences in Epipona guerini represent dipha- sic allometry, which necessarily indicates preimaginal caste determination. Such di- morphism is also known in Agelaia (Ag. fla- vipennis, Evans and West-Eberhard, 1970; Ag. areata, Jeanne and Fagen, 1974; Ag. pal- lipes and Ag. multipicta, Noll et al., 1997; Ag. vicina, Sakagami et al., 1996; Baio et al., 1998), Apoica (Apoica flavissima, Shima et al., 1994; Noll and Zucchi, 2002; Ap. pal- lens, Jeanne et al., 1995), Chartergus globi- ventris (Noll and Zucchi, 2002), Protonec-
16 AMERICAN MUSEUM NOVITATES
tarina sylveirae (Shima et al., 1996b, 2003), Protopolybia (Protopolybia exigua, Noll et al., 1996; Noll and Zucchi, 2002; Pr. acutis- cutis, cited as Pr. pumila, Naumann, 1970), Polybia (Polybia occidentalis, Richards and Richards, 1951; Noll et al., 2000; Po. bis- triata, Richards and Richards 1951; Po. ema- ciata, Hebling and Letizio, 1973; Po. dimi- diata, Maule-Rodrigues and Santos, 1974; Shima et al., 1996a; Po. paulista and Po. scutellaris, Noll and Zucchi, 2000), and Pseudopolybia difficilis (Jeanne, 1996). In the present study, different regression lines for queens and workers indicate different de- velopmental paths in certain species, some more strongly than others. There is clear dis- tinction for Polybia liliacea and Epipona ta- tua, somewhat less clear for species where queens are mostly larger, such as Polybia spi- nifex, Po. rejecta, and Chartergus metano- talis, while regressions for Charterginus ful- vus are based on relatively few data (fig. 3). Note that the plot of Epipona tatua closely matches that of E. guerini from Hunt et al. (1996), so although the evidence for prei- maginal determination in Epipona is less dis- tinct than for certain other species (say, Po- lybia liliacea), it is found in different species of the genus and therefore is probably real. INTERMEDIACY: Even though preimaginal caste determination is well documented in a number of species (above), in others repro- ductive and nonreproductive females cannot be distinguished by morphology. Ovarian status itself may also be continuous such that there is no discrete separation of females. Richards and Richards (1951) referred to noninseminated females with developed ova- ries as “‘intermediates’’. Uninseminated lay- ers can be found in species with some mor- phological caste differentiation such as Pro- topolybia exigua (fig. 5; Simdes, 1977; Noll et al., 1997) so that these females are clearly workers (fig. 5). West-Eberhard (1978) sug- gested that females of worker status would benefit by keeping their ovaries active, even if all their eggs were eaten, because laying workers could attempt to be new queens in the next colony founded by absconding or normal swarms. However, in species where castes are indistinct to begin with (e.g., Brachygastra lecheguana, fig. 5, Shima et al., 2000), intermediates present a challenge
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to the concept of caste itself because they further obscure the difference between repro- ductives and nonreproductives. After all, there can be no meaningful “‘caste’’ if there is no meaningful difference between females. As mentioned above, terms such as “laying worker’ or “‘replacement queen” do not serve to clarify the situation if worker and queen castes are not already distinct. Strass- mann et al. (2002) named the situation in which any female may possibly become an egglayer in the event of loss of some queens as “‘caste totipotency’’. The term is some- what of an oxymoron if “‘caste’’ itself means anything. The problem is that the concept of caste is being stretched to mean different things in different situations.
SYNTHESIS: Reproductive castes are not the same from species to species in Epiponini. Some interpretable patterns form when we capture the diversity in terms of simple mor- phometrics (fig. 5), but there is little explan- atory power in a plot of canonical covariance and reproductive status. This is partly be- cause the details of evolution are overspeci- fied in the morphometric data. For example, the idea that queens should have proportion- ally larger abdomens and smaller heads is both classical and logical (Jeanne and Fagen, 1975; Yamane et al., 1983), but it does not specify which dimensions of the head or ab- domen should change most noticeably. Sim- ilarly, Wheeler’s (1991) model stated that isomorphic species would develop size-based differences in developmental patterns, but it does not specify what body dimensions will differ to fulfill diphasic allometry. Wheeler’s model would be considered valid if different measures in different species satisfied the prediction, because the model is based on the evolution of a syndrome (i.e., the evolution of a number of different characters that are expected to change in loose synchrony). To interpret the current data, we need to reduce the details of our analysis to compose syn- dromes so that the broad patterns of evolu- tion are not lost in the metric details. Table 1 represents just an effort at defining syn- dromes, with categories following Richards’ (1978) concepts based on individual mea- sures. However, our treatment of the covari- ance terms and intermediate females (see the discussion of fig. 5, and above) permits us to
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Primitive monomorphic species
no morphological caste physiological caste
=n Se _
reproductives larger, intermediates different shapes w/ no intermediates
NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 17
Apoica Angiopolybia Pseudopolybia
Parachartergus
[ Chartergellus
Nectarinella Leipomeles Synoeca Clypearia Metapolybia Asteloeca Protopolybia Charterginus
Chartergus
Brachygastra Protonectarina Epipona Polybia spp.
ke P. liliaceat+ P. dimidiata
queens smaller in some aspects
Fig. 6. Caste syndromes defined by data of table 1 and ovarian dissection, optimized on cladogram of Wenzel and Carpenter. Where genera are polymorphic for caste syndrome, terminals are coded ac-
cording to parsimonious optimization.
reformulate Richards’ syndromes and add one more. We propose the following groups: (1) casteless (no size or shape difference as- sociated with reproduction, females of all ovarian conditions present); (2) physiological caste only (no morphometric differences, but ovarian condition unambiguous by absence of type C females); (3) queens larger but mostly the same shape; (4) queens shaped differently with some measures smaller than workers. Although further research may find this list (or characterization of given species within the list) to be incomplete, we show
below that a powerful and coherent pattern emerges from this perspective.
Figure 6 represents the working cladogram to date for Epiponini, from the cladogram of Wenzel and Carpenter (1994), rooted to a hy- pothetical ancestor that is without morpho- logical caste (Polistes, Mischocyttarus, etc.). Generic synonymies published since 1994 have been incorporated here (Clypearia = Occipitalia, Carpenter et al., 1996; Polybia = Synoecoides, Carpenter et al., 2000; Lei- pomeles = Marimbonda, Carpenter, in press). The original cladogram was reported
18 AMERICAN MUSEUM NOVITATES
from analysis of Carpenter’s (1991) morpho- logical matrix of 31 characters (including a few traditional behavioral characters) and from Wenzel’s (1993) matrix of 21 behav- ioral or nest architectural characters, not overlapping with those of Carpenter. None of the matrix characters included information about caste. The relevant caste syndromes, as defined above, are plotted on the cladogram and optimized parsimoniously to hypotheti- cal ancestors. While figure 5 suggests a spray of points in a continuum, the historical lin- eages are marked rather neatly in blocks in figure 6. The Epiponini in general is char- acterized as primitively casteless. Retaining this primitive absence of caste, Angiopolybia pallens, Pseudopolybia vespiceps, Parachar- tergus fraternus, P. smithii, Leipomeles dor- sata, Chartergellus communis, and Nectari- nella championi all have high Wilks’ lambda value and poor queen—worker distinction (fig. 5). Without clear morphological caste, Synoeca, Clypearia, Asteloeca, and Metapo- lybia aztecoides have distinct physiological differences (but notice morphological varia- tion in M. docilis, fig. 5). This is the syn- drome we have added to Richards’ three, and if it were simply synonymized with “‘no mor- phological difference’’ then the absence of caste is even more definitively shown to be the ancestral condition for Epiponini. Some Polybia and related genera have queens larg- er, and a few species of Polybia have queens with some dimensions smaller, the final syn- drome. This last syndrome is also found in Apoica (table 1). Agelaia vicina, Ag. palli- pes, Ag. multipicta, and other species in the literature (table 1) also have developed queens of different shape.
The most conspicuous feature of figure 6 is that the interpretation of caste is rather simple. Interestingly, the syndromes as de- fined by morphological and physiological distinctions map rather neatly to traditional groups as recognized by gross nest architec- ture. At the foundation are the genera that have covered nests and brood combs sup- ported by pedicels (“‘calyptodomous, stelo- cyttarus”’ Richards, 1978; Wenzel, 1993; An- giopolybia to Nectarinella). The genera that build with cells directly on the substrate (Synoeca to Asteloeca, the ‘“‘astelocyttarus”’ design of Richards) have physiological caste
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only, while the more apical “‘phragmocytta- rus’’ nest builders have the more sophisticat- ed caste systems. If the syndromes them- selves are used as a character of the taxa and combined with the matrices of Carpenter (1991) and Wenzel (1993), then different trees result. Figure 7 shows the principal dif- ference, which is that Apoica and A gelaia be- come sisters in a lineage basal to the remain- der of Epiponini. This is because the shape difference of queens is enough to unite them, and it constitutes a more parsimonious plot, with only two derivations of queens smaller in some measure than workers, one in the Apoica-Agelaia lineage and one in Polybia liliacea + Po. dimidiata. Future research will test if Apoica and Agelaia are actually sisters. It seems that different models offered by Wheeler (1991) and Jeanne et al. (1995) are both fulfilled in different parts of the clado- gram, and that one syndrome has not been accounted for in previous models. The pro- posal from Jeanne et al. (1995) is fulfilled in that Apoica derived queens of different shape without first developing different size, either alone (fig. 6) or with its sister Agelaia (fig. 7), which may have derived size differences independently.
Wheeler’s (1991) more extensive model is fairly direct and general. Our explanation is derived simply from hers. Wheeler started with monophasic variation, meaning that the same allometric relationships operate across a continuous spread of sizes (fig. 8A). One can imagine that the first step to distinct castes is that the continuity in size is inter- rupted, producing individuals that differ in size and perhaps in behavioral role (fig. 8B). Once this distinction becomes regular, then it would be easy to select for developmental switches that create different allometric re- lationships in the two size classes, meaning that the large and smallbody-size classes dif- fer in fundamental shape, as well as in size, generating discrete and disjunct variation (fig. 8C). As the efficiency of the switch is improved by operating earlier in develop- ment, final gross body size may become ir- relevant, and castes could be produced such that they differ in morphology but not in size (fig. 8D). Such switches are already known in Apis, where the fate of a larva is deter- mined early, and final body size is not causal
2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 19
Angiopolybia
Pseudopolybia Parachartergus ne [ Chartergellus
Nectarinella
Leipomeles Synoeca Clypearia he “e"" Metapolybi Primitive |__| A eee : monomorphic Charterginus species Protopolybia Chartergus Brachygastra no morphological caste Protonectarina physiological caste Epipona Polybia spp. t= P. liliacea + P. dimidiata
a
reproductives larger, intermediates ems (ifferent shapes w/ no intermediates === queens smaller in some aspects
Fig. 7. Caste syndromes defined as in fig. 6, optimized on cladogram produced by using caste syndrome as a character in combination with the matrix of Wenzel and Carpenter.
A B C D we 7 Casteless Queens larger Developmental Castes differ
switch allometrically
Fig. 8. Wheeler’s (1991) model of the evolution of caste, stepwise in graphical terms, representing morphometric variation measured within a colony. See text for explanation.
20 AMERICAN MUSEUM NOVITATES
to caste determination (Evans and Wheeler, 1999). The presence of the predicted devel- opmental switch in Apis is encouraging, but the best corroboration of the model would be to find evidence of the same stepwise pro- cedure as outlined above in a rich dataset. Our cladograms (figs. 6, 7) with caste syn- drome optimized on them provide exactly this opportunity. Tracing along the bottom- most lineage, which subtends the major path of genus-level diversity, demonstrates that in social wasps there does appear to be stepwise development of the sort necessary to corrob- orate the model. Casteless societies give rise to those that differ in size, which give rise to those that differ in shape, and some of these include queens that are smaller (hence, a dis- sociation of size and morphological identity). Thus, the patterns we describe here include the predictions of Wheeler’s model, even considering the necessary placement of in- termediate states. We think that this is the first empirical validation of Wheeler’s model to date.
Neither models by Jeanne et al. (1995) nor Wheeler (1991) anticipated the discovery of “physiological caste only’’ as reported here, a group where ovary development is clear, with no persistent intermediates. The clade that includes Synoeca and Asteloeca (fig. 6) has rather distinct reproductives upon dissec- tion, but discrimination is weak based on our measures. These results are difficult to inter- pret, but the cladistic coherence of the syn- drome suggests that it is not an artifact. To propose that this result is somehow errone- ous is a great stretch, because that would re- quire that it is only accidental that multivar- iate statistics find similar patterns among measures from different colonies in different genera in different studies; that it is acciden- tal that only these species were united despite a field of other possibilities; that it is acci- dental that these species all fall out in a cla- distically interpretable pattern; and accidental that this pattern matches that of the tradition- al “‘astelocyttarus’’ nest architecture (see Wenzel [1991, 1993, 1998] for discussion of nest form). The physiological switch that de- termines reproductivity in this group is not yet understood, but “‘cyclical oligogyny”’ was discovered in this group and may pro- vide a key. West Eberhard (1978) reported
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that queen number in Metapolybia is reduced in part through workers challenging queens, and this may eliminate intermediate females as well if the selection criterion is based on an estimate of fecundity. As such, queen se- lection by workers would seem to represent an important social behavior that produces selection pressure to have an abrupt switch from nonreproductive to reproductive, and in this clade it is separate from considerations of size or shape, unlike Polybia and other derived genera. Organization of labor in Me- tapolybia is also known to differ from that of Polybia, being more simple (Karsai and Wenzel, 1998; cf. Jeanne, 1986), and perhaps this ‘‘astelocyttarus’’ clade has been over- looked for important transitional forms in other ways as well.
CONCLUSIONS
This analysis indicates that caste has evolved in different ways in different line- ages of Epiponini, starting from casteless so- cieties. Our decision to call the basal condi- tion “‘casteless”’ relies on two independent lines of argument. The first argument is that females do not differ meaningfully either in morphology or physiology. The second is that the reproductives do not represent dom- inant animals, as they do in more primitive societies such as those of Polistes and Mis- chocyttarus. As discussed above, workers are known to police the egglayers in Apoica, Synoeca, and Metapolybia, whereas the eg- glayer herself polices the brood comb in Pol- istes. Thus, the egglayers of the genera rep- resented by the groups of Angiopolybia through Nectarinella, and Synoeca through Asteloeca do not represent the same social role as egglayers in Polistes; instead, they are simply individuals that lay eggs in a society of females that are not otherwise distin- guished. This may not have been recognized before because, despite universal acceptance of Hamiltonian perspectives regarding inclu- sive fitness, the community of vespid re- searchers still imagines wasps engaged in a struggle for direct fitness rather than joined in a society of inclusive fitness. It seems like- ly that different types of socio-regulation ex- ist in epiponines as suggested by Noll and Zucchi (2002). It is possible that some con-
2004
fusion results in the literature from a desire to find a single syndrome to be representative of the entire diversity of swarming wasps, whereas the actual evolution of caste has per- haps been multifaceted.
ACKNOWLEDGMENTS
We thank Jim Carpenter for suggestions on the manuscript, Sidnei Mateus for his un- selfish expertise in fieldtrips and friendship, the OSU Social Insects Discussion Group for commentary, and financial support from OSU Research Foundation, Fapesp (Funda- ¢ao de Amparo a Pesquisa do Estado de Sao Paulo) grant no. 01-02491-4 and CNPq.
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