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PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3467, 24 pp., 8 ®gures, 10 tables December 30, 2004

Evolution of Caste in Neotropical Swarm-Founding (: ; )

FERNANDO B. NOLL,1 JOHN W. WENZEL,2 AND RONALDO ZUCCHI3

ABSTRACT Reproductive castes are compared in species of swarming wasps representing all currently recognized genera of Epiponini (). 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 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 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 . are accompanied by physiological and mor-

1 Departamento de Zoologia e BotaÃnica; Instituto de BiocieÃncias, Letras e CieÃncias Exatas, UNESP; Rua CristoÂvaÄo Colombo, 2265; 15054-000, SaÄo Jose do Rio Preto, SP; ([email protected]). 2 Department of Entomology, The Ohio State University, 1315 Kinnear Road, Columbus, OH 43212 (wenzel. [email protected]). 3 Departamento de Biologia, Faculdade de Filoso®a CieÃncias e Letras de RibeiraÄo Preto, Universidade de SaÄo Paulo, Brazil ([email protected]).

Copyright ᭧ American Museum of Natural History 2004 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3467 phological specializations and body-size var- diversity that can be arranged along a spec- iation (Oster and Wilson, 1978). The degree trum from taxa in which queens and workers to which castes are distinct often serves as are externally similar, to others with fairly part of the de®nition of the society itself, distinct caste attributes (reviewed in with greater caste differentiation indicating O'Donnell, 1998; Shima et al., 1998). The ``higher'' sociality (Bourke, 1999). In some Paleotropical tribe Ropalidini (perhaps the groups, such as swarm-founding neotropical sister to the Neotropical tribe Epiponini ex- wasps, the species are described as highly so- amined here) shows diversity that is hard to cial, although the distinction between queens interpret without more study. For instance, and workers is considered slight and often some species of Ropalidia present distinct confusing (Richards and Richards, 1951; morphological castes (Yamane et al., 1983), Richards, 1978, cited as Polybiini, junior including those of small colony size (Wenzel, synonym of Epiponini, see Carpenter, 1993, 1992), but others show morphologically sim- 1997). ilar castes despite larger colony size (Gad- Wasps (Hymenoptera: Vespidae) have fre- agkar and Joshi, 1982, 1983; Yamane and quently been used to test evolutionary mod- ItoÃ, 1987; Gadagkar, 1987). Parapolybia has els for the origin of social behavior because castes (Yamane and Maeta, 1985) but their of their different levels of socialityÐfrom behavior is poorly known. Belonogaster is solitary to eusocial (West-Eberhard, 1978, also poorly known (Pardi and Piccioli, 1981) 1996; Wilson, 1985; ItoÃ, 1986; Spradbery, but is thought to show great morphological 1991). General theory holds that primitive variation (Keeping, 2000, 2002). In Poly- systems of dominance rely on physical ag- bioides, morphological castes are known in gression, with the winner becoming the eg- P. tabidus (Turillazzi et al., 1994), which glayer. More derived systems require some builds large colonies and reproduces by kind of caste determination that may occur swarms. However, despite the repeated evo- during the immature stages of an individual's lution of castes in social wasps as a whole, development (preimaginal determination), the evolution of castes is largely interpreted with an unambiguous physiological or mor- through our understanding of Epiponini. phological result that cannot be reversed. Ab- Epiponini is a tribe of Polistinae, with sence of morphological castes is a plesiom- about 20 well-marked genera and at least 229 orphic (``primitive'') condition in the three species, plus another 27 subspecies, all of subfamilies of social wasps, so that morpho- which are Neotropical. All Epiponini are po- logical castes were attained independently in lygynic (meaning that many queens com- different lineages (Carpenter, 1991). Most monly reproduce simultaneously on the same distant to the question at hand, females of nest), and all reproduce by swarms, which is Stenogastrinae are barely distinguished as taken as a sign of sophisticated, obligatory, queens or as workers (Turillazzi, 1991). high sociality. Initially, Richards (1978) doc- Closer, and sister to the subfamily examined umented three forms of caste discrimination, here, queens of Vespinae are larger than and recent research builds upon these: (1) workers (Spradbery, 1991), but such a trait Queens larger than workers. In some species may be an adaptation for a queen's solitary caste differences are so pronounced that they winter survival in most species (West-Eber- must be determined by nutritional differences hard, 1978). In the Polistinae (studied here), during larval development (Evans and West- the most basal genera (Polistes and Mischo- Eberhard, 1970; Jeanne and Fagen, 1974; cyttarus), initiate their nests solitarily, with Sakagami et al., 1996; Noll et al., 1997), with egglayers only slightly larger than non-eg- important consequences for fertility and re- glayers. However, polistines present a large productive asymmetries (West-Eberhard, 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 3

1978; O'Donnell, 1998). The classical land- TABLE 1 mark is a case of different, nonallometric Morphometric Differences Reported from Literature castes of 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 dif®- 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, 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 dif®cult 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 4 AMERICAN MUSEUM NOVITATES NO. 3467 phase of colony cycle that was measured, SaÄo Paulo, Brazil, and the AMNH. They particularly when the colony was collected were taken by being put into a plastic bag opportunistically by visitors on brief ®eld- provided with ether-moistened cotton balls or trips. In addition, when reproductive status with open cyanide tubes. Populations were ®xed in Dietrich's solution and then kept in does not relate closely to morphological var- 70% ethanol for dissection. iation, there is a tendency to rescue a concept From each of these colonies 100 workers of caste by categorizing problematic females and all queens were measured and dissected. as ``laying workers'' or ``replacement When castes could be discriminated by size queens'' on an ad hoc basis. Such axiomatic or color, all possible queens were selected, descriptions may serve only to obscure the and from the remaining individuals 100 original question, protecting an inadequate workers were arbitrarily selected. In small concept of caste itself from refutation by em- colonies where castes were not obvious, all pirical data. We address these issues by pre- individuals were measured and dissected. In large colonies where castes were hard to senting here the most complete set of com- identify, 100 individuals were chosen ran- parable values regarding caste determination. domly. After identifying some morphological A total of more than 13,500 measures en- characters to discriminate queens, such as ab- compassing nine dimensions of 13 species dominal size, all individuals having such a are offered for the ®rst time. These are in- pattern were chosen and used in the analysis. tegrated with comparable data from other The following characters were measured un- studies to include 68 species. We establish der a binocular microscope (smallest unit ϭ the basal condition for Epiponini, providing 0.01 mm): head width (HW), minimum in- evidence for both preimaginal and postima- terorbital distance (IDm), gena width (GW), width of mesoscutum (MSW), alitrunk ginal caste determination. In addition to mor- length (AL), length of gastral tergite I (T1L), phometric variation in caste, we stress the ex- basal height of T (T BH), basal widths of istence of various types of social regulation. 1 1 tergite II (T2BW), and partial length of the forewing (WL) (®g. 1, for more details about MATERIALS AND METHODS the characters see Shima et al., 1994). Ovary Workers and queens were taken from ma- condition was determined under a stereomi- ture colonies (i.e., post worker emergence) of croscope. In order to analyze insemination, 13 different species of Epiponini collected in the spermatheca was removed and put on a three different localities. Angiopolybia pal- slide in a 1:1 solution of glycerin and ethanol lens (Lepeletier), Asteloeca ujhelyii (Ducke), (70%). The presence of sperm cells was con- Charterginus fulvus Fox, Clypearia sulcata ®rmed by microscope. (de Saussure), and Leipomeles dorsata (Fa- Before statistical analysis, data were con- bricius) were collected in Iquitos, . Nec- verted to millimeters and later converted by tarinella championi (Dover) was collected in log transformation in order to avoid prob- Costa Rica, near Atenas. For these two lo- lems of variance. Means and standard devi- calities, the samples were collected by John ations were calculated from the nine mor- W. Wenzel and James Carpenter, killed in cy- phological measurements. Statistical charac- anide and preserved promptly in 70% etha- terization of caste was explored in two ways. nol, and deposited in the AMNH. One-way ANOVA was used for comparisons (Polybia) liliacea (Fabricius), Polybia (For- of means to demonstrate whether castes (as micicola) rejecta (Fabricius), Chartergus me- determined by dissection) differ in some tanotalis Richards, Epipona tatua (Cuvier), body dimensions. Because multiple measures Metapolybia aztecoides Richards, Polybia that relate to shape are not always captured (Pedothoeca) spinifex Richards, and well in single comparisons, stepwise discrim- surinama (Linnaeus) were collected in Nova inant function analysis was used to see if Xavantina, Mato Grosso, Brazil by Fernando combinations of variables could be useful in B. Noll and Sidnei Mateus. Vouchers are de- predicting caste. In this method, variables are posited at the Museu de Zoologia (MZUSP), successively added to the model based on the 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 5

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 (T1L), basal height of T1 (T1BH), basal widths of tergite II (T2BW), and partial length of the forewing (WL). higher F to enter values, adding no more var- based on the effectiveness in previous pub- iables when the F-ratio is no longer signi®- lications (Jeanne et al., 1995; Jeanne, 1996; cant. However, variables that enter the model Hunt et al., 1996). early may be completely subsumed by sep- arate variables that enter later. The signi®- RESULTS cance of Wilks' lambda (an estimate of com- OVARIAN DEVELOPMENT mon variance between sets of variates) was used to determine the degree to which sep- The ovariole number was always three in arate measures contributed to the ®nal model. each ovary, and the following types of ovar- This is an alternative to using an F to remove ian development were distinguished (table at each step. Variables that appear in the ®nal 2); type A: with ®lamentous ovarioles that model but do not have signi®cant F-ratios had no visible oocytes or with some very represent variance components that are ex- small oocytes; type B: bearing some young plained by some combination of the other oocytes; type C: with one or more mature variables also in the model, and therefore no oocytes in each ovariole; type D: with well- longer contribute to the discrimination itself. developed and very long ovarioles coiled in- Wilks' lambda varies from zero to one: the side the gaster, with at least one mature egg. lower the value, the greater the signi®cance. Only females with type D ovaries were in- Analysis of covariance (ANCOVA) was seminated. All four types were found in the used, with alitrunk length (AL) as a covari- following species: , ate, in order to identify different growth rates Charterginus fulvus, Leipomeles dorsata, in the body parts measured. AL was chosen and Nectarinella championi (table 2). Type 6 AMERICAN MUSEUM NOVITATES NO. 3467

TABLE 2 queens (tables 3±6). Univariate statistics Ovary Development for All Species Analyzeda (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 ®rst group (®g. 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 (table 4). AN- OVA showed no signi®cant differences in any measurement in An. pallens, As. ujhelyii, and Cl. sulcata;inS. surinama, only one measurement was signi®cant, and in L. dor- C was not found in Asteloeca ujhelyii, Char- sata, M. aztecoides, and N. championi three tergus metanotalis, Occipitalia sulcata, Epi- measurements were signi®cant. Except for pona tatua, Metapolybia aztecoides, Polybia M. aztecoides, in which some characters liliacea, Polybia rejecta, Polybia spinifex, were smaller in queens than in workers, dif- and Synoeca surinama (table 2). Queens' ova- ferences were always based on queens being ries (type D, inseminated) were much longer larger than workers. ANCOVA, using ali- than workers' ovaries in Chartergus metano- trunk length as a dependent variable (table talis, Epipona tatua, Polybia liliacea, Polybia 7), was not signi®cant in any character in An. rejecta, and Polybia spinifex. No species of pallens, As. ujhelyii, and Cl. sulcata.InL. this study lacked both types B and C. dorsata, M. aztecoides, N. championi, and S. surinama, signi®cant differences were de- MORPHOLOGICAL DIFFERENCES tected. Differences of mean values of nine char- Wilks' lambda values were used to infer acters measured were tested in workers and 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 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 7

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

TABLE 5 Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of Charterginus fulvus, Chartergus metanotalis, and Epipona tatua 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

to the model that predicts the caste of the surements had a low power of discrimination individual wasps. Signi®cance values of the in Cn. fulvus, Cg. metanotalis, and E. tatua loadings of each morphometric variable in- (tables 8, 9), and that discrimination between dicate whether that variable contributes castes can only occur based on a combination meaningfully to the prediction of caste. Anal- of measurements. In Polybia rejecta and Po. ysis showed that, in the above species, spinifex, differences were much more pro- Wilks' lambda values were always high, nounced and all measurements were stronger ranging from 0.7 to 1.0 (table 8). Consider- discriminators. Wilks' lambda ranged from ing that lambda is de®ned as 1.0 minus the 0.1 to 0.3 (table 9), and castes were more squared canonical correlation, the highest clearly discriminated than in the previous value is 1.0, indicating complete absence of group (table 10). ANCOVA showed signi®- association. These data indicate that morpho- cant differences in growth rates of body parts logical castes are practically absent in these in at least one character in all species of this species, based on these measures. Speci®cal- group (table 7). ly, even if queens may differ from workers In a third class, Polybia liliacea castes on average, the ability to identify an individ- were as clearly distinct as in the second ual as a queen or worker based on morpho- group, but head width was smaller in queens metric values is very poor. None of the than in workers (table 6). ANOVA showed queens were correctly classi®ed by discrim- that all measurements were different between inant scores in An. pallens or Cl. sulcata, and queens and workers. relatively few in L. dorsata, M. aztecoides, N. championi, and S. surinama (see table 10). DISCUSSION Only in As. ujhelyii are castes better discrim- inated. A distinct physiological separation of fe- In a second group (®g. 3)ÐCharterginus males into those that are reproductive and fulvus, Chartergus metanotalis, Epipona ta- those that are nonreproductive is possible tua, Polybia rejecta, and P. spinifexÐqueens based on ovarian condition and insemination were larger than workers. Mean differences in some of the species reported here. While using ANOVA (tables 5, 6) were found in complete absence of ovarian development in ®ve of nine characters in Cn. fulvus and Cg. workers (i.e., the absence of both types B and metanotalis.InE. tatua, Po. rejecta, and Po. C) was not found in the species studied here, spinifex all body measurements were differ- such a syndrome has been reported in Apoica ent. ¯avissima, (Sakagami et al., Multivariate analysis showed that the mea- 1996), Ag. pallipes, and Ag. multipicta (Noll 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 9

Fig. 2. Slight caste discrimination found in some epiponines based mostly on shape (when appli- cable). Individuals identi®ed by dissection to be ``queens'' are represented as squares, while those identi®ed 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' pallipes and Ag. multipicta (Noll et al., ovaries (type D) were much longer than 1997). Similarly, though less discrete, inter- workers' ovaries in Chartergus metanotalis, mediate type C was not found in Asteloeca Epipona tatua, Polybia liliacea, Po. rejecta, ujhelyii, Chartergus metanotalis, Clypearia and Po. spinifex. This situation is also known sulcata, Epipona tatua, Metapolybia aztecoi- in Apoica ¯avissima (Shima et al., 1994), des, Polybia liliacea, Po. rejecta, Po. spini- sylveirae (Shima et al., fex, and Synoeca surinama (table 2). Other 1996a), Polybia dimidiata (Shima et al., species previously reported to have similar 1996b), Po. scutellaris, Po. paulista and Po. distinction are Protonectarina sylveirae (Shi- occidentalis (Noll and Zucchi, 2000), Age- ma et al., 1996a), Polybia dimidiata (Shima laia vicina (Sakagami et al., 1996), and Ag. et al., 1996b), Po. scutellaris and Po. paulis- TABLE 7 Covariance Analyses Using Alitrunk Length as Covariate for the Analyzed Species

TABLE 8 Wilks' Lambda and F-Statistics Lambda values estimate the degree of contribution for each separate measure to the ®nal discriminant function model. In these cases values were between 1.0 and about 0.5, indicating low discrimination of castes. F-statistics for ANOVA using the same variables are shown, with appropriate signi®cance values. 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 11

Fig. 3. Caste discrimination found in some epiponines based on size and shape. Individuals identi®ed by dissection to be ``queens'' are represented as squares, while those identi®ed 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 ®nal 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 signi®cance values. 12 AMERICAN MUSEUM NOVITATES NO. 3467

TABLE 10 Classi®cation Scores for Group Comparisons Using Discriminant Analysis

ta (Noll and Zucchi, 2000), and Chartergus Ovarian development presents a confusing globiventris (Noll and Zucchi, 2002). Some array of conditions, yet previous researchers species are found to have individuals repre- have tried to ®nd ways to capture the totality senting all four stages, implying a near con- of this variation with some kind of overarch- tinuum (but that insemination is always as- ing hypothesis of caste that would be applied sociated with type D ovaries). These species to all species of Epiponini equally. For ex- include Angiopolybia pallens, Charterginus ample, the concept of cyclical oligogyny in- fulvus, Leipomeles dorsata, and Nectarinella vokes demography to provide a process by championi (table 2). The same pattern, im- which individuals may become queens at plying a lack of physiological caste in any swarm initiation of colonies, but not later in meaningful way, was previously found in the colony cycle (West Eberhard, 1978). Col- other species using the same procedure, such ony cycle is known to relate to the degree of as communis (Mateus et al., morphological differentiation in species that 1999), Pseudopolybia vespiceps (Shima et do have marked differences, with differences al., 1998), smithii (Mateus et growing as colonies age (e.g., Noll and Zuc- al., 1997), and lecheguana chi, 2000, 2002), and comparing mature col- (Shima et al., 2000). onies is now required if one is to argue that 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 13 the that are sampled actually repre- among adults rather than by larval manipu- sent the species' breadth of morphological lation. Young females have their ovaries sup- diversity. Nonetheless, the search for a single pressed in queen-right colonies, so that only explanation of caste (its presence or its am- through orphanage do young females develop biguity) in Epiponini is still lacking. We offer their ovaries and become queens (West-Eber- here a novel view that relies on returning to hard, 1978). In such species, caste as a phys- the fundamental question of whether caste iological state may be distinct even if it is exists at all. We then integrate the answers impossible to recognize morphologically. Of to those questions to provide the most co- particular interest may be Astleoca ujhelyii.In herent view of caste to date, one that does table 10 there is fairly good discrimination of not seek to explain all Epiponini through a reproductive ``queens'' and nonreproductive single fundamental process. ``workers'', with from 10 or 20% error. Table 8 shows that two values contribute signi®- MORPHOMETRIC DIFFERENCES BETWEEN cantly to the discriminant function model, CASTES meaning that the computer can ®nd a way to separate reproductives and nonreproductives Size divergence is usually regarded as an if they are labeled prior to analysis. However, initial step for the origin of morphological table 3 shows that none of the linear metrics castes in the three main groups of social Hy- are signi®cantly different between castes (see menoptera (ants, bees, and wasps; Wheeler, also ®g. 2 for graphic representation of over- 1991). In wasps, caste-related size differenc- lap). Thus, this species presents a kind of in- es are conspicuous in the Vespinae, but com- termediate state in which reproductive status plex in the Polistinae (®g. 4). However, the can be explained by shape differences after practice of comparing ratios of linear body the fact, but not predicted based on the nine measures (®g. 4) may be overly simple to morphometric variables independently, in- capture the actual patterns of caste determi- cluding variables that are adequate to capture nation. For this reason, we used not only lin- caste in other species (see below). Asteloeca ear measures themselves, but also analysis of ujhelyii occupies a region of parameter space their covariance to look for shape differences that represents a shift between species with associated with reproductive status as well as distinct reproductive castes and those that are size differences. casteless morphologically. In general, morphometric differences asso- Species of Epiponini appear to represent a ciated with ovarian status were either slight or continuum from those without morphological absent in Angiopolybia pallens, Asteloeca castes (above) to those with discrete castes ujhelyii, Clypearia sulcata (table 3), Leipo- (below). There are now enough data to dem- meles dorsata, Metapolybia aztecoides, Nec- onstrate this by presenting measures from tarinella championi, and Synoeca surinama species analyzed by the same protocols, (table 4). Other studies found the same for whether in the present study or in the liter- Parachartergus smithii (Mateus et al., 1997), ature. Plotting the percentage of queens cor- Pa. colobopterus (Strassmann et al., 1991), rectly classi®ed by discriminant function Pseudopolybia vespiceps (Shima et al., 1998), analysis (table 10, and literature) versus Chartergellus communis (Mateus et al., Wilks' lambda values (table 8 and 9, and lit- 1999), (Shima et erature), we see that in many species queens al., 2000), Synoeca cyanea (Noda et al., are classi®ed correctly from 80 to 100% of 2003), and Metapolybia docilis (Baio et al., the time, while in other species classi®cation 2003a). In this group, we might say that while is less effective (®g. 5). Breaking the contin- some individuals are reproductive and some uum of ®gure 5 into logical parts, we ®nd are not, there is no meaningful morphological that species with low Wilks' lambda for mor- caste. In some cases, caste appears to be what phometric variables (i.e., they show strong Kukuk (1994) called behaviorally eusocially covariance between morphometric measures determined in the adult stage. In Metapolybia and ovarian status) can be classi®ed correctly and Synoeca (West-Eberhard, 1978, 1981), most of the time (®g. 5, region A). Distinc- caste is apparently determined by disputes tions between reproductive and nonreproduc- 14 AMERICAN MUSEUM NOVITATES NO. 3467

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 ¯avissima, 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. ru®ceps, 47. Po. scutellaris, 48. Po. singularis, 49. Po. spinifex, 50. Po. striata, 51. Protonectarina sylveirae, 52. , 53. Pr. minu- tissima, 54. Pr. pumilla, 55. Pr. sedula, 56. Pseudopolybia dif®cilis, 57. Ps. vespiceps, 58. Synoeca cyanea, 59. S. surinama, 60. Vespula squamosa. For references for the species, see table 1. tive females may represent a general increase dle of the continuum (®g. 5, region B) are in all measures (e.g., Polybia rejecta or Po. species such as Asteloeca ujhelyii with high spinifex, ®g. 3, table 5) or in some measures Wilks' lambdas (weak covariance between more than others such that there is a con- measures and ovarian status). These may be spicuous shape difference as well (dramati- without conspicuous size differences (®g. 2, cally in Polybia liliacea, where queens are table 3; ®g. 5, region B; Asteloeca ujhelyii), larger in all ways, except with smaller heads but shape differences are enough to permit in absolute terms, ®g. 3, table 6). In the mid- effective classi®cation of reproductives 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 15

Fig. 5. Plots of Wilks' lambda values versus queens correctly classi®ed using discriminant function analysis for some epiponines. See text for discussion. nonetheless. These species that can be cor- well as in several other epiponines (see be- rectly classi®ed as queens or workers (®g. 5, low), the nature of queen±worker differences regions A and B) show that there is no gen- would be determined during the larval stage eral rule for identifying reproductives, be- such that queen-destined larvae show differ- cause the way queens differ in shape from ent growth rates of various compartments workers varies between species (tables 8, 9). compared to worker-destined larvae, gener- Finally, in some species reproductives do not ating animals of different shape even though differ substantially in size or shape (e.g., An- they are about the same size. In several spe- giopolybia pallens, table 3, Nectarinella cies, not only shape but also size is involved, championi, table 4; ®g. 2 and table 8; ®g. 5, perhaps as a secondary acquisition (Jeanne, region C). 1996: Hunt et al. 1996). SHAPE: It has long been known that repro- Hunt et al. (1996) proposed that shape dif- ductive status in Epiponini is not strongly as- ferences in Epipona guerini represent dipha- sociated with body size for many species. In- sic allometry, which necessarily indicates deed, the claim that morphological castes had preimaginal caste determination. Such di- arisen without a primordial size component morphism is also known in Agelaia (Ag. ¯a- was ®rst made for social wasps (Jeanne et vipennis, Evans and West-Eberhard, 1970; al., 1995). Castes in differed Ag. areata, Jeanne and Fagen, 1974; Ag. pal- signi®cantly in body proportions but not in lipes and Ag. multipicta, Noll et al., 1997; overall size. Such a ®nding indicates that Ag. vicina, Sakagami et al., 1996; Baio et al., morphological castes may not have their or- 1998), Apoica (Apoica ¯avissima, Shima et igins in a single allometric growth function al., 1994; Noll and Zucchi, 2002; Ap. pal- along a body size gradient (Jeanne et al., lens, Jeanne et al., 1995), Chartergus globi- 1995). It seems that in Apoica pallens,as ventris (Noll and Zucchi, 2002), Protonec- 16 AMERICAN MUSEUM NOVITATES NO. 3467 tarina sylveirae (Shima et al., 1996b, 2003), to the concept of caste itself because they Protopolybia (Protopolybia exigua, Noll et further obscure the difference between repro- al., 1996; Noll and Zucchi, 2002; Pr. acutis- ductives and nonreproductives. After all, cutis, cited as Pr. pumila, Naumann, 1970), there can be no meaningful ``caste'' if there Polybia (, Richards and is no meaningful difference between females. Richards, 1951; Noll et al., 2000; Po. bis- As mentioned above, terms such as ``laying triata, Richards and Richards 1951; Po. ema- worker'' or ``replacement queen'' do not ciata, Hebling and LetõÂzio, 1973; Po. dimi- serve to clarify the situation if worker and diata, Maule-Rodrigues and Santos, 1974; queen castes are not already distinct. Strass- Shima et al., 1996a; Po. paulista and Po. mann et al. (2002) named the situation in scutellaris, Noll and Zucchi, 2000), and which any female may possibly become an Pseudopolybia dif®cilis (Jeanne, 1996). In egglayer in the event of loss of some queens the present study, different regression lines as ``caste totipotency''. The term is some- for queens and workers indicate different de- what of an oxymoron if ``caste'' itself means velopmental paths in certain species, some anything. The problem is that the concept of more strongly than others. There is clear dis- caste is being stretched to mean different tinction for Polybia liliacea and Epipona ta- things in different situations. tua, somewhat less clear for species where SYNTHESIS: Reproductive castes are not the queens are mostly larger, such as Polybia spi- same from species to species in Epiponini. nifex, Po. rejecta, and Chartergus metano- Some interpretable patterns form when we talis, while regressions for Charterginus ful- capture the diversity in terms of simple mor- vus are based on relatively few data (®g. 3). phometrics (®g. 5), but there is little explan- Note that the plot of Epipona tatua closely atory power in a plot of canonical covariance matches that of E. guerini from Hunt et al. and reproductive status. This is partly be- (1996), so although the evidence for prei- cause the details of evolution are overspeci- maginal determination in Epipona is less dis- ®ed in the morphometric data. For example, tinct than for certain other species (say, Po- the idea that queens should have proportion- lybia liliacea), it is found in different species ally larger abdomens and smaller heads is of the genus and therefore is probably real. both classical and logical (Jeanne and Fagen, INTERMEDIACY: Even though preimaginal 1975; Yamane et al., 1983), but it does not caste determination is well documented in a specify which dimensions of the head or ab- number of species (above), in others repro- domen should change most noticeably. Sim- ductive and nonreproductive females cannot ilarly, Wheeler's (1991) model stated that be distinguished by morphology. Ovarian isomorphic species would develop size-based status itself may also be continuous such that differences in developmental patterns, but it there is no discrete separation of females. does not specify what body dimensions will Richards and Richards (1951) referred to differ to ful®ll diphasic allometry. Wheeler's noninseminated females with developed ova- model would be considered valid if different ries as ``intermediates''. Uninseminated lay- measures in different species satis®ed the ers can be found in species with some mor- prediction, because the model is based on the phological caste differentiation such as Pro- evolution of a syndrome (i.e., the evolution topolybia exigua (®g. 5; SimoÄes, 1977; Noll of a number of different characters that are et al., 1997) so that these females are clearly expected to change in loose synchrony). To workers (®g. 5). West-Eberhard (1978) sug- interpret the current data, we need to reduce gested that females of worker status would the details of our analysis to compose syn- bene®t by keeping their ovaries active, even dromes so that the broad patterns of evolu- if all their eggs were eaten, because laying tion are not lost in the metric details. Table workers could attempt to be new queens in 1 represents just an effort at de®ning syn- the next colony founded by absconding or dromes, with categories following Richards' normal swarms. However, in species where (1978) concepts based on individual mea- castes are indistinct to begin with (e.g., sures. However, our treatment of the covari- Brachygastra lecheguana, ®g. 5, Shima et ance terms and intermediate females (see the al., 2000), intermediates present a challenge discussion of ®g. 5, and above) permits us to 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 17

Fig. 6. Caste syndromes de®ned 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 below that a powerful and coherent pattern one more. We propose the following groups: emerges from this perspective. (1) casteless (no size or shape difference as- Figure 6 represents the working cladogram sociated with reproduction, females of all to date for Epiponini, from the cladogram of ovarian conditions present); (2) physiological Wenzel and Carpenter (1994), rooted to a hy- caste only (no morphometric differences, but pothetical ancestor that is without morpho- ovarian condition unambiguous by absence logical caste (Polistes, , etc.). of type C females); (3) queens larger but Generic synonymies published since 1994 mostly the same shape; (4) queens shaped have been incorporated here (Clypearia ϭ differently with some measures smaller than Occipitalia, Carpenter et al., 1996; Polybia workers. Although further research may ®nd ϭ Synoecoides, Carpenter et al., 2000; Lei- this list (or characterization of given species pomeles ϭ Marimbonda, Carpenter, in within the list) to be incomplete, we show press). The original cladogram was reported 18 AMERICAN MUSEUM NOVITATES NO. 3467 from analysis of Carpenter's (1991) morpho- only, while the more apical ``phragmocytta- logical matrix of 31 characters (including a rus'' nest builders have the more sophisticat- few traditional behavioral characters) and ed caste systems. If the syndromes them- from Wenzel's (1993) matrix of 21 behav- selves are used as a character of the taxa and ioral or nest architectural characters, not combined with the matrices of Carpenter overlapping with those of Carpenter. None of (1991) and Wenzel (1993), then different the matrix characters included information trees result. Figure 7 shows the principal dif- about caste. The relevant caste syndromes, as ference, which is that Apoica and Agelaia be- de®ned above, are plotted on the cladogram come sisters in a lineage basal to the remain- and optimized parsimoniously to hypotheti- der of Epiponini. This is because the shape cal ancestors. While ®gure 5 suggests a spray difference of queens is enough to unite them, of points in a continuum, the historical lin- and it constitutes a more parsimonious plot, eages are marked rather neatly in blocks in with only two derivations of queens smaller ®gure 6. The Epiponini in general is char- in some measure than workers, one in the acterized as primitively casteless. Retaining Apoica-Agelaia lineage and one in Polybia this primitive absence of caste, Angiopolybia liliacea ϩ Po. dimidiata. Future research will pallens, Pseudopolybia vespiceps, Parachar- test if Apoica and Agelaia are actually sisters. tergus fraternus, P. smithii, Leipomeles dor- It seems that different models offered by sata, Chartergellus communis, and Nectari- Wheeler (1991) and Jeanne et al. (1995) are nella championi all have high Wilks' lambda both ful®lled in different parts of the clado- value and poor queen±worker distinction gram, and that one syndrome has not been (®g. 5). Without clear morphological caste, accounted for in previous models. The pro- Synoeca, Clypearia, Asteloeca, and Metapo- posal from Jeanne et al. (1995) is ful®lled in lybia aztecoides have distinct physiological that Apoica derived queens of different shape differences (but notice morphological varia- without ®rst developing different size, either tion in M. docilis, ®g. 5). This is the syn- alone (®g. 6) or with its sister Agelaia (®g. drome we have added to Richards' three, and 7), which may have derived size differences if it were simply synonymized with ``no mor- independently. phological difference'' then the absence of Wheeler's (1991) more extensive model is caste is even more de®nitively shown to be fairly direct and general. Our explanation is the ancestral condition for Epiponini. Some derived simply from hers. Wheeler started Polybia and related genera have queens larg- with monophasic variation, meaning that the er, and a few species of Polybia have queens same allometric relationships operate across with some dimensions smaller, the ®nal syn- a continuous spread of sizes (®g. 8A). One drome. This last syndrome is also found in can imagine that the ®rst step to distinct Apoica (table 1). Agelaia vicina, Ag. palli- castes is that the continuity in size is inter- pes, Ag. multipicta, and other species in the rupted, producing individuals that differ in literature (table 1) also have developed size and perhaps in behavioral role (®g. 8B). queens of different shape. Once this distinction becomes regular, then it The most conspicuous feature of ®gure 6 would be easy to select for developmental is that the interpretation of caste is rather switches that create different allometric re- simple. Interestingly, the syndromes as de- lationships in the two size classes, meaning ®ned by morphological and physiological that the large and smallbody-size classes dif- distinctions map rather neatly to traditional fer in fundamental shape, as well as in size, groups as recognized by gross nest architec- generating discrete and disjunct variation ture. At the foundation are the genera that (®g. 8C). As the ef®ciency of the switch is have covered nests and brood combs sup- improved by operating earlier in develop- ported by pedicels (``calyptodomous, stelo- ment, ®nal gross body size may become ir- cyttarus'' Richards, 1978; Wenzel, 1993; An- relevant, and castes could be produced such giopolybia to Nectarinella). The genera that that they differ in morphology but not in size build with cells directly on the substrate (®g. 8D). Such switches are already known (Synoeca to Asteloeca, the ``astelocyttarus'' in Apis, where the fate of a is deter- design of Richards) have physiological caste mined early, and ®nal body size is not causal 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 19

Fig. 7. Caste syndromes de®ned as in ®g. 6, optimized on cladogram produced by using caste syndrome as a character in combination with the matrix of Wenzel and Carpenter.

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 NO. 3467 to caste determination (Evans and Wheeler, that queen number in Metapolybia is reduced 1999). The presence of the predicted devel- in part through workers challenging queens, opmental switch in Apis is encouraging, but and this may eliminate intermediate females the best corroboration of the model would be as well if the selection criterion is based on to ®nd evidence of the same stepwise pro- an estimate of fecundity. As such, queen se- cedure as outlined above in a rich dataset. lection by workers would seem to represent Our cladograms (®gs. 6, 7) with caste syn- an important social behavior that produces drome optimized on them provide exactly selection pressure to have an abrupt switch this opportunity. Tracing along the bottom- from nonreproductive to reproductive, and in most lineage, which subtends the major path this clade it is separate from considerations of genus-level diversity, demonstrates that in of size or shape, unlike Polybia and other social wasps there does appear to be stepwise derived genera. Organization of labor in Me- development of the sort necessary to corrob- tapolybia is also known to differ from that orate the model. Casteless societies give rise of Polybia, being more simple (Karsai and to those that differ in size, which give rise to Wenzel, 1998; cf. Jeanne, 1986), and perhaps those that differ in shape, and some of these this ``astelocyttarus'' clade has been over- include queens that are smaller (hence, a dis- looked for important transitional forms in sociation of size and morphological identity). other ways as well. Thus, the patterns we describe here include the predictions of Wheeler's model, even CONCLUSIONS considering the necessary placement of in- termediate states. We think that this is the This analysis indicates that caste has ®rst empirical validation of Wheeler's model evolved in different ways in different line- to date. ages of Epiponini, starting from casteless so- Neither models by Jeanne et al. (1995) nor cieties. Our decision to call the basal condi- Wheeler (1991) anticipated the discovery of tion ``casteless'' relies on two independent ``physiological caste only'' as reported here, lines of argument. The ®rst argument is that a group where ovary development is clear, females do not differ meaningfully either in with no persistent intermediates. The clade morphology or physiology. The second is that includes Synoeca and Asteloeca (®g. 6) that the reproductives do not represent dom- has rather distinct reproductives upon dissec- inant animals, as they do in more primitive tion, but discrimination is weak based on our societies such as those of Polistes and Mis- measures. These results are dif®cult to inter- chocyttarus. As discussed above, workers are pret, but the cladistic coherence of the syn- known to police the egglayers in Apoica, drome suggests that it is not an artifact. To Synoeca, and Metapolybia, whereas the eg- propose that this result is somehow errone- glayer herself polices the brood comb in Pol- ous is a great stretch, because that would re- istes. Thus, the egglayers of the genera rep- quire that it is only accidental that multivar- resented by the groups of Angiopolybia iate statistics ®nd similar patterns among through Nectarinella, and Synoeca through measures from different colonies in different Asteloeca do not represent the same social genera in different studies; that it is acciden- role as egglayers in Polistes; instead, they are tal that only these species were united despite simply individuals that lay eggs in a society a ®eld of other possibilities; that it is acci- of females that are not otherwise distin- dental that these species all fall out in a cla- guished. This may not have been recognized distically interpretable pattern; and accidental before because, despite universal acceptance that this pattern matches that of the tradition- of Hamiltonian perspectives regarding inclu- al ``astelocyttarus'' nest architecture (see sive ®tness, the community of vespid re- Wenzel [1991, 1993, 1998] for discussion of searchers still imagines wasps engaged in a nest form). The physiological switch that de- struggle for direct ®tness rather than joined termines reproductivity in this group is not in a society of inclusive ®tness. It seems like- yet understood, but ``cyclical oligogyny'' ly that different types of socio-regulation ex- was discovered in this group and may pro- ist in epiponines as suggested by Noll and vide a key. West Eberhard (1978) reported Zucchi (2002). It is possible that some con- 2004 NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS 21 fusion results in the literature from a desire MoÈbius, 1856 (Hymenoptera: Vespidae; Polis- to ®nd a single syndrome to be representative tinae), and a new key to the genera of paper of the entire diversity of swarming wasps, wasps of the New World. American Museum whereas the actual evolution of caste has per- Novitates. haps been multifaceted. Carpenter, J.M., J.I. Kojima, and J.W. Wenzel. 2000. Polybia, paraphyly, and polistine phylog- eny. American Museum Novitates 3298: 24 pp. ACKNOWLEDGMENTS Carpenter, J.M., and K.G. Ross. 1984. Colony composition in four special of Polistinae from We thank Jim Carpenter for suggestions on Suriname, with a description of the larva of the manuscript, Sidnei Mateus for his un- Brachygastra scutellaris (Hymenoptera, Ves- sel®sh expertise in ®eldtrips and friendship, pidae). Psyche 91: 237±250. the OSU Social Insects Discussion Group for Carpenter, J.M., J.W. Wenzel, and J. Kojima. commentary, and ®nancial support from 1996. Synonymy of the genus Occipitalia Rich- OSU Research Foundation, Fapesp (Funda- ards, 1978, with Clypearia de Saussure 1854 cËaÄo de Amparo aÁ Pesquisa do Estado de SaÄo (Hymenoptera: Vespidae; Polistinae, Epiponi- Paulo) grant no. 01-02491-4 and CNPq. ni). Journal of Hymenoptera Research 5: 157± 165. Evans, H.E., and M.J. West-Eberhard. 1970. The REFERENCES wasps. Ann Arbor, MI: University of Michigan Baio, M.V., F.B. Noll, R. Zucchi, and D. SimoÄes. Press, vii ϩ 265 pp. 1998. Non-allometric caste differences in Age- Evans, J.D., and D.E. Wheeler. 1999. Differential laia vicina (Hymenoptera, Vespidae, Epiponi- gene expression between developing queens ni). Sociobiology 34: 465±476. and workers in the honey bee, Apis mellifera. Baio, M.V., F.B. Noll, and R. Zucchi. 2003a. 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