Evolution of Caste in Neotropical Swarm Founding Wasps (Hymenoptera: Vespidae; Epiponini): 10 Tables

Copyright q American Museum of Natural History 2004 ISSN 0003-0082

P U B L I S H E D B Y T H E A M E R I C A N M U S E U M O F N AT U R A L H I S T O RY

CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024

Number 3467, 24 pp., 8 figures, 10 tables December 30, 2004

Evolution of Caste in NeotropicalSwarm-Founding Wasps

(Hymenoptera: Vespidae; Epiponini)

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

ABSTRACT

Reproductive castes are compared in species of swarming wasps representing all currentlyrecognized genera of Epiponini (Polistinae). New morphometric data for nine measures ofbody parts and ovarian data are presented for 13 species. These are integrated with all similarlyconducted available studies, giving a total of 30 species. Analysis reveals several syndromesrelating reproductive and nonreproductive individuals: no meaningful distinction, physiologicaldifferences 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 syndromesamong 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 acasteless society that is not comparable to the primitively social genus Polistes where dominantqueens control reproduction. Castes originate several times in Epiponini, with different resultsin different lineages. The best documented evolutionary sequence passes from casteless so-cieties, to those with reproductives larger, to those with reproductives differing in shape fromnonreproductives, to those with reproductives smaller in some measures. This sequence isconsistent with Wheeler’s theory of the origin of caste through developmental switches, andrepresents the most thorough test of that theory to date.

INTRODUCTION

Separation into castes is one of the cor-nerstones of the evolution of social insects.

1 Departamento de Zoologia e Botanica; Instituto de Biociencias, Letras e Ciencias Exatas, UNESP; Rua CristovaoColombo, 2265; 15054-000, Sao Jose do Rio Preto, SP; Brazil ([email protected]).

2 Department of Entomology, The Ohio State University, 1315 Kinnear Road, Columbus, OH 43212 ([email protected]).

3 Departamento de Biologia, Faculdade de Filosofia Ciencias e Letras de Ribeirao Preto, Universidade de SaoPaulo, Brazil ([email protected]).

In some species, reproductive ‘‘queens’’ andnonreproductive ‘‘workers’’ differ only inbehavior, but in other species such behaviorsare accompanied by physiological and mor-

2 NO. 3467AMERICAN MUSEUM NOVITATES

phological specializations and body-size var-iation (Oster and Wilson, 1978). The degreeto which castes are distinct often serves aspart of the definition of the society itself,with greater caste differentiation indicating‘‘higher’’ sociality (Bourke, 1999). In somegroups, such as swarm-founding neotropicalwasps, the species are described as highly so-cial, although the distinction between queensand workers is considered slight and oftenconfusing (Richards and Richards, 1951;Richards, 1978, cited as Polybiini, juniorsynonym of Epiponini, see Carpenter, 1993,1997).

Wasps (Hymenoptera: Vespidae) have fre-quently been used to test evolutionary mod-els for the origin of social behavior becauseof their different levels of sociality—fromsolitary to eusocial (West-Eberhard, 1978,1996; Wilson, 1985; Ito, 1986; Spradbery,1991). General theory holds that primitivesystems of dominance rely on physical ag-gression, with the winner becoming the eg-glayer. More derived systems require somekind of caste determination that may occurduring the immature stages of an individual’sdevelopment (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 threesubfamilies of social wasps, so that morpho-logical castes were attained independently indifferent lineages (Carpenter, 1991). Mostdistant to the question at hand, females ofStenogastrinae are barely distinguished asqueens or as workers (Turillazzi, 1991).Closer, and sister to the subfamily examinedhere, queens of Vespinae are larger thanworkers (Spradbery, 1991), but such a traitmay be an adaptation for a queen’s solitarywinter 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, withegglayers only slightly larger than non-eg-glayers. However, polistines present a large

diversity that can be arranged along a spec-trum from taxa in which queens and workersare externally similar, to others with fairlydistinct caste attributes (reviewed inO’Donnell, 1998; Shima et al., 1998). ThePaleotropical tribe Ropalidini (perhaps thesister to the Neotropical tribe Epiponini ex-amined here) shows diversity that is hard tointerpret without more study. For instance,some species of Ropalidia present distinctmorphological 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 andIto, 1987; Gadagkar, 1987). Parapolybia hascastes (Yamane and Maeta, 1985) but theirbehavior is poorly known. Belonogaster isalso poorly known (Pardi and Piccioli, 1981)but is thought to show great morphologicalvariation (Keeping, 2000, 2002). In Poly-bioides, morphological castes are known inP. tabidus (Turillazzi et al., 1994), whichbuilds large colonies and reproduces byswarms. However, despite the repeated evo-lution of castes in social wasps as a whole,the evolution of castes is largely interpretedthrough our understanding of Epiponini.

Epiponini is a tribe of Polistinae, withabout 20 well-marked genera and at least 229species, plus another 27 subspecies, all ofwhich are Neotropical. All Epiponini are po-lygynic (meaning that many queens com-monly reproduce simultaneously on the samenest), and all reproduce by swarms, which istaken 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 speciescaste differences are so pronounced that theymust be determined by nutritional differencesduring larval development (Evans and West-Eberhard, 1970; Jeanne and Fagen, 1974;Sakagami et al., 1996; Noll et al., 1997), withimportant consequences for fertility and re-productive asymmetries (West-Eberhard,

2004 3NOLL ET AL.: CASTES IN NEOTROPICAL SWARM-FOUNDING WASPS

TABLE 1Morphometric Differences Reported from

Literature

1978; O’Donnell, 1998). The classical land-mark is a case of different, nonallometriccastes of Agelaia areata, where queens andworkers have different shapes as well as dif-ferent sizes (Jeanne and Fagen, 1974). Itseems that these differences must representpreimaginal bias in nutrition. (2) Allometricdifferences, 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 etal., 1995), according to the idea that the bodyplans represent fundamentally different endproducts, not different points along a contin-uum. Sometimes such castes are barely de-tectable (Jeanne, 1996). (3) Slight or indis-tinct morphological differences, with castesabsent, or manifested weakly, based on onlya few traits (Richards, 1978; Jeanne, 1980).One great problem is that integration of theempirical studies is not straightforward be-cause few studies are exactly comparable inmeasurement methodology or phase of col-ony cycle studied, so generalization is diffi-cult. A rough summary of species known tofall into these three conditions can be foundin 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 genusin Epiponini. However, Apoica is peculiarand 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 notbe a good model of basal synapomorphies ofEpiponini. It has not been demonstrated thatpreimaginal determination is the basal con-dition for the whole clade.

Integrating studies of caste in Epiponini isdifficult because studies to date have beenlimited in scope, with most publications cov-ering one species at a time. Measurementsare not necessarily comparable across stud-ies. There are sometimes doubts about the


phase of colony cycle that was measured,particularly when the colony was collectedopportunistically by visitors on brief field-trips. In addition, when reproductive statusdoes not relate closely to morphological var-iation, there is a tendency to rescue a conceptof caste by categorizing problematic femalesas ‘‘laying workers’’ or ‘‘replacementqueens’’ on an ad hoc basis. Such axiomaticdescriptions may serve only to obscure theoriginal question, protecting an inadequateconcept 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 speciesare offered for the first time. These are in-tegrated with comparable data from otherstudies to include 68 species. We establishthe basal condition for Epiponini, providingevidence 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) of13 different species of Epiponini collected inthree 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 inCosta Rica, near Atenas. For these two lo-calities, the samples were collected by JohnW. 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 Synoecasurinama (Linnaeus) were collected in NovaXavantina, Mato Grosso, Brazil by FernandoB. Noll and Sidnei Mateus. Vouchers are de-posited at the Museu de Zoologia (MZUSP),

Sao Paulo, Brazil, and the AMNH. Theywere taken by being put into a plastic bagprovided with ether-moistened cotton balls orwith open cyanide tubes. Populations werefixed in Dietrich’s solution and then kept in70% ethanol for dissection.

From each of these colonies 100 workersand all queens were measured and dissected.When castes could be discriminated by sizeor color, all possible queens were selected,and from the remaining individuals 100workers were arbitrarily selected. In smallcolonies where castes were not obvious, allindividuals were measured and dissected. Inlarge colonies where castes were hard toidentify, 100 individuals were chosen ran-domly. After identifying some morphologicalcharacters to discriminate queens, such as ab-dominal size, all individuals having such apattern were chosen and used in the analysis.The following characters were measured un-der a binocular microscope (smallest unit 50.01 mm): head width (HW), minimum in-terorbital distance (IDm), gena width (GW),width of mesoscutum (MSW), alitrunklength (AL), length of gastral tergite I (T1L),basal height of T1 (T1BH), basal widths oftergite II (T2BW), and partial length of theforewing (WL) (fig. 1, for more details aboutthe characters see Shima et al., 1994). Ovarycondition was determined under a stereomi-croscope. In order to analyze insemination,the spermatheca was removed and put on aslide 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 bylog 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 comparisonsof means to demonstrate whether castes (asdetermined by dissection) differ in somebody dimensions. Because multiple measuresthat relate to shape are not always capturedwell in single comparisons, stepwise discrim-inant function analysis was used to see ifcombinations of variables could be useful inpredicting caste. In this method, variables aresuccessively added to the model based on the


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 partiallength 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 modelearly 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) wasused to determine the degree to which sep-arate measures contributed to the final model.This is an alternative to using an F to removeat each step. Variables that appear in the finalmodel but do not have significant F-ratiosrepresent variance components that are ex-plained by some combination of the othervariables also in the model, and therefore nolonger contribute to the discrimination itself.Wilks’ lambda varies from zero to one: thelower the value, the greater the significance.

Analysis of covariance (ANCOVA) wasused, with alitrunk length (AL) as a covari-ate, in order to identify different growth ratesin 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 ineach ovary, and the following types of ovar-ian development were distinguished (table2); type A: with filamentous ovarioles thathad no visible oocytes or with some verysmall oocytes; type B: bearing some youngoocytes; type C: with one or more matureoocytes 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 thefollowing species: Angiopolybia pallens,Charterginus fulvus, Leipomeles dorsata,and Nectarinella championi (table 2). Type


TABLE 2Ovary Development for All Species Analyzeda

TABLE 3Means and Observed Values of ANOVA Test, for Nine Characters Used for Discriminating Castes of

Angiopolybia pallens, Asteloeca ujhelyii, and Clypearia sulcata

C was not found in Asteloeca ujhelyii, Char-tergus metanotalis, Occipitalia sulcata, Epi-pona tatua, Metapolybia aztecoides, Polybialiliacea, Polybia rejecta, Polybia spinifex,and Synoeca surinama (table 2). Queens’ ova-ries (type D, inseminated) were much longerthan workers’ ovaries in Chartergus metano-talis, Epipona tatua, Polybia liliacea, Polybiarejecta, and Polybia spinifex. No species ofthis study lacked both types B and C.

MORPHOLOGICAL DIFFERENCES

Differences of mean values of nine char-acters measured were tested in workers and

queens (tables 3–6). Univariate statistics(ANOVA) showed that measured characterscould be different or not between queens andworkers in different species. Also, based onmultivariate statistics, the power of discrim-ination of each measurement varied in thedifferent 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 inany measurement in An. pallens, As. ujhelyii,and Cl. sulcata; in S. surinama, only onemeasurement was significant, and in L. dor-sata, M. aztecoides, and N. championi threemeasurements were significant. Except forM. aztecoides, in which some characterswere smaller in queens than in workers, dif-ferences were always based on queens beinglarger than workers. ANCOVA, using ali-trunk length as a dependent variable (table7), 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 inferthe independent contribution of each variable



Leipomeles dorsata, Metapolybia aztecoides, Nectarinella championi, and Synoeca surinama


Charterginus fulvus, Chartergus metanotalis, and Epipona tatua


TABLE 6Means 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 theindividual wasps. Significance values of theloadings of each morphometric variable in-dicate whether that variable contributesmeaningfully 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 thesquared canonical correlation, the highestvalue is 1.0, indicating complete absence ofassociation. These data indicate that morpho-logical castes are practically absent in thesespecies, based on these measures. Specifical-ly, even if queens may differ from workerson average, the ability to identify an individ-ual as a queen or worker based on morpho-metric values is very poor. None of thequeens were correctly classified by discrim-inant scores in An. pallens or Cl. sulcata, andrelatively 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)—Charterginusfulvus, Chartergus metanotalis, Epipona ta-tua, Polybia rejecta, and P. spinifex—queenswere larger than workers. Mean differencesusing ANOVA (tables 5, 6) were found infive 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 discriminationin Cn. fulvus, Cg. metanotalis, and E. tatua(tables 8, 9), and that discrimination betweencastes can only occur based on a combinationof measurements. In Polybia rejecta and Po.spinifex, differences were much more pro-nounced and all measurements were strongerdiscriminators. Wilks’ lambda ranged from0.1 to 0.3 (table 9), and castes were moreclearly discriminated than in the previousgroup (table 10). ANCOVA showed signifi-cant differences in growth rates of body partsin at least one character in all species of thisgroup (table 7).

In a third class, Polybia liliacea casteswere as clearly distinct as in the secondgroup, but head width was smaller in queensthan in workers (table 6). ANOVA showedthat all measurements were different betweenqueens and workers.

DISCUSSION

A distinct physiological separation of fe-males into those that are reproductive andthose that are nonreproductive is possiblebased on ovarian condition and inseminationin some of the species reported here. Whilecomplete absence of ovarian development inworkers (i.e., the absence of both types B andC) was not found in the species studied here,such a syndrome has been reported in Apoicaflavissima, Agelaia vicina (Sakagami et al.,1996), Ag. pallipes, and Ag. multipicta (Noll


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 thoseidentified as ‘‘workers’’ are solid dots. Separate regression lines are drawn for illustration only; see textfor discussion.

et al., 1997). In our present study, queens’ovaries (type D) were much longer thanworkers’ ovaries in Chartergus metanotalis,Epipona tatua, Polybia liliacea, Po. rejecta,and Po. spinifex. This situation is also knownin 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 Asteloecaujhelyii, Chartergus metanotalis, Clypeariasulcata, Epipona tatua, Metapolybia aztecoi-des, Polybia liliacea, Po. rejecta, Po. spini-fex, and Synoeca surinama (table 2). Otherspecies previously reported to have similardistinction are Protonectarina sylveirae (Shi-ma et al., 1996a), Polybia dimidiata (Shimaet al., 1996b), Po. scutellaris and Po. paulis-

TA

BL

E7

Cov

aria

nce

An

alys

esU

sin

gA

litr

un

kL

engt

has

Cov

aria

tefo

rth

eA

nal

yzed

Sp

ecie

s

TA

BL

E8

Wil

ks’

Lam

bd

aan

dF

-Sta

tist

ics

Lam

bda

valu

eses

tim

ate

the

degr

eeof

cont

ribu

tion

for

each

sepa

rate

mea

sure

toth

efi

nal

disc

rim

inan

tfu

ncti

onm

odel

.In

thes

eca

ses

valu

esw

ere

betw

een

1.0

and

abou

t0.

5,in

dica

ting

low

disc

rim

inat

ion

ofca

stes

.F

-sta

tist

ics

for

AN

OV

Aus

ing

the

sam

eva

riab

les

are

show

n,w

ith

appr

opri

ate

sign

ifica

nce

valu

es.


Fig. 3. Caste discrimination found in some epiponines based on size and shape. Individuals identifiedby dissection to be ‘‘queens’’ are represented as squares, while those identified as ‘‘workers’’ are soliddots. Separate regression lines are drawn for illustration only; see text for discussion.

TABLE 9Wilks’ Lambda and F-Statistics

Lambda values estimate the degree of contribution for each separate measure to the final discriminant functionmodel. In these cases values were about 0.5 and lower, indicating better discrimination if compared tothose found in table 8. F-statistics for ANOVA using the same variables are shown, with appropriate

significance values.


TABLE 10Classification Scores for Group Comparisons Using Discriminant Analysis

ta (Noll and Zucchi, 2000), and Chartergusglobiventris (Noll and Zucchi, 2002). Somespecies 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 speciesinclude Angiopolybia pallens, Charterginusfulvus, Leipomeles dorsata, and Nectarinellachampioni (table 2). The same pattern, im-plying a lack of physiological caste in anymeaningful way, was previously found inother species using the same procedure, suchas Chartergellus communis (Mateus et al.,1999), Pseudopolybia vespiceps (Shima etal., 1998), Parachartergus smithii (Mateus etal., 1997), and Brachygastra lecheguana(Shima et al., 2000).

Ovarian development presents a confusingarray of conditions, yet previous researchershave tried to find ways to capture the totalityof this variation with some kind of overarch-ing hypothesis of caste that would be appliedto all species of Epiponini equally. For ex-ample, the concept of cyclical oligogyny in-vokes demography to provide a process bywhich individuals may become queens atswarm initiation of colonies, but not later inthe colony cycle (West Eberhard, 1978). Col-ony cycle is known to relate to the degree ofmorphological differentiation in species thatdo have marked differences, with differencesgrowing 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


the animals that are sampled actually repre-sent the species’ breadth of morphologicaldiversity. Nonetheless, the search for a singleexplanation of caste (its presence or its am-biguity) in Epiponini is still lacking. We offerhere a novel view that relies on returning tothe fundamental question of whether casteexists at all. We then integrate the answersto those questions to provide the most co-herent view of caste to date, one that doesnot seek to explain all Epiponini through asingle fundamental process.

MORPHOMETRIC DIFFERENCES BETWEEN

CASTES

Size divergence is usually regarded as aninitial step for the origin of morphologicalcastes 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, thepractice of comparing ratios of linear bodymeasures (fig. 4) may be overly simple tocapture the actual patterns of caste determi-nation. For this reason, we used not only lin-ear measures themselves, but also analysis oftheir covariance to look for shape differencesassociated with reproductive status as well assize differences.

In general, morphometric differences asso-ciated with ovarian status were either slight orabsent in Angiopolybia pallens, Asteloecaujhelyii, Clypearia sulcata (table 3), Leipo-meles dorsata, Metapolybia aztecoides, Nec-tarinella championi, and Synoeca surinama(table 4). Other studies found the same forParachartergus 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 etal., 2000), Synoeca cyanea (Noda et al.,2003), and Metapolybia docilis (Baio et al.,2003a). In this group, we might say that whilesome individuals are reproductive and someare not, there is no meaningful morphologicalcaste. In some cases, caste appears to be whatKukuk (1994) called behaviorally eusociallydetermined in the adult stage. In Metapolybiaand Synoeca (West-Eberhard, 1978, 1981),caste is apparently determined by disputes

among adults rather than by larval manipu-lation. Young females have their ovaries sup-pressed in queen-right colonies, so that onlythrough orphanage do young females developtheir ovaries and become queens (West-Eber-hard, 1978). In such species, caste as a phys-iological state may be distinct even if it isimpossible to recognize morphologically. Ofparticular interest may be Astleoca ujhelyii. Intable 10 there is fairly good discrimination ofreproductive ‘‘queens’’ and nonreproductive‘‘workers’’, with from 10 or 20% error. Table8 shows that two values contribute signifi-cantly to the discriminant function model,meaning that the computer can find a way toseparate reproductives and nonreproductivesif they are labeled prior to analysis. However,table 3 shows that none of the linear metricsare significantly different between castes (seealso fig. 2 for graphic representation of over-lap). Thus, this species presents a kind of in-termediate state in which reproductive statuscan be explained by shape differences afterthe fact, but not predicted based on the ninemorphometric variables independently, in-cluding variables that are adequate to capturecaste in other species (see below). Asteloecaujhelyii occupies a region of parameter spacethat represents a shift between species withdistinct reproductive castes and those that arecasteless morphologically.

Species of Epiponini appear to represent acontinuum from those without morphologicalcastes (above) to those with discrete castes(below). There are now enough data to dem-onstrate this by presenting measures fromspecies 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 functionanalysis (table 10, and literature) versusWilks’ lambda values (table 8 and 9, and lit-erature), we see that in many species queensare classified correctly from 80 to 100% ofthe time, while in other species classificationis less effective (fig. 5). Breaking the contin-uum of figure 5 into logical parts, we findthat species with low Wilks’ lambda for mor-phometric variables (i.e., they show strongcovariance between morphometric measuresand ovarian status) can be classified correctlymost of the time (fig. 5, region A). Distinc-tions between reproductive and nonreproduc-


Fig. 4. Comparison of the level of caste distinction between epiponines (1–59, white circles indicateworkers with ovarian development, black diamonds indicate workers without ovarian development) anda Vespinae (60, black square) based on wing length queen–worker ratio versus length of tergite I (except14, 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. Clypeariasulcata, 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. platycephasylvestris, 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. Synoecacyanea, 59. S. surinama, 60. Vespula squamosa. For references for the species, see table 1.

tive females may represent a general increasein all measures (e.g., Polybia rejecta or Po.spinifex, fig. 3, table 5) or in some measuresmore than others such that there is a con-spicuous shape difference as well (dramati-cally in Polybia liliacea, where queens arelarger in all ways, except with smaller headsin absolute terms, fig. 3, table 6). In the mid-

dle of the continuum (fig. 5, region B) arespecies such as Asteloeca ujhelyii with highWilks’ lambdas (weak covariance betweenmeasures and ovarian status). These may bewithout conspicuous size differences (fig. 2,table 3; fig. 5, region B; Asteloeca ujhelyii),but shape differences are enough to permiteffective classification of reproductives


Fig. 5. Plots of Wilks’ lambda values versus queens correctly classified using discriminant functionanalysis 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 fromworkers varies between species (tables 8, 9).Finally, in some species reproductives do notdiffer substantially in size or shape (e.g., An-giopolybia pallens, table 3, Nectarinellachampioni, 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 hadarisen without a primordial size componentwas first made for social wasps (Jeanne etal., 1995). Castes in Apoica pallens differedsignificantly in body proportions but not inoverall size. Such a finding indicates thatmorphological castes may not have their or-igins in a single allometric growth functionalong 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 differenceswould be determined during the larval stagesuch that queen-destined larvae show differ-ent growth rates of various compartmentscompared to worker-destined larvae, gener-ating animals of different shape even thoughthey 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 indicatespreimaginal 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 etal., 1994; Noll and Zucchi, 2002; Ap. pal-lens, Jeanne et al., 1995), Chartergus globi-ventris (Noll and Zucchi, 2002), Protonec-


tarina sylveirae (Shima et al., 1996b, 2003),Protopolybia (Protopolybia exigua, Noll etal., 1996; Noll and Zucchi, 2002; Pr. acutis-cutis, cited as Pr. pumila, Naumann, 1970),Polybia (Polybia occidentalis, Richards andRichards, 1951; Noll et al., 2000; Po. bis-triata, Richards and Richards 1951; Po. ema-ciata, Hebling and Letızio, 1973; Po. dimi-diata, Maule-Rodrigues and Santos, 1974;Shima et al., 1996a; Po. paulista and Po.scutellaris, Noll and Zucchi, 2000), andPseudopolybia difficilis (Jeanne, 1996). Inthe present study, different regression linesfor queens and workers indicate different de-velopmental paths in certain species, somemore strongly than others. There is clear dis-tinction for Polybia liliacea and Epipona ta-tua, somewhat less clear for species wherequeens 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 closelymatches 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 speciesof the genus and therefore is probably real.

INTERMEDIACY: Even though preimaginalcaste determination is well documented in anumber of species (above), in others repro-ductive and nonreproductive females cannotbe distinguished by morphology. Ovarianstatus itself may also be continuous such thatthere is no discrete separation of females.Richards and Richards (1951) referred tononinseminated 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; Simoes, 1977; Nollet al., 1997) so that these females are clearlyworkers (fig. 5). West-Eberhard (1978) sug-gested that females of worker status wouldbenefit by keeping their ovaries active, evenif all their eggs were eaten, because layingworkers could attempt to be new queens inthe next colony founded by absconding ornormal swarms. However, in species wherecastes are indistinct to begin with (e.g.,Brachygastra lecheguana, fig. 5, Shima etal., 2000), intermediates present a challenge

to the concept of caste itself because theyfurther obscure the difference between repro-ductives and nonreproductives. After all,there can be no meaningful ‘‘caste’’ if thereis no meaningful difference between females.As mentioned above, terms such as ‘‘layingworker’’ or ‘‘replacement queen’’ do notserve to clarify the situation if worker andqueen castes are not already distinct. Strass-mann et al. (2002) named the situation inwhich any female may possibly become anegglayer in the event of loss of some queensas ‘‘caste totipotency’’. The term is some-what of an oxymoron if ‘‘caste’’ itself meansanything. The problem is that the concept ofcaste is being stretched to mean differentthings in different situations.

SYNTHESIS: Reproductive castes are not thesame from species to species in Epiponini.Some interpretable patterns form when wecapture the diversity in terms of simple mor-phometrics (fig. 5), but there is little explan-atory power in a plot of canonical covarianceand 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 isboth classical and logical (Jeanne and Fagen,1975; Yamane et al., 1983), but it does notspecify which dimensions of the head or ab-domen should change most noticeably. Sim-ilarly, Wheeler’s (1991) model stated thatisomorphic species would develop size-baseddifferences in developmental patterns, but itdoes not specify what body dimensions willdiffer to fulfill diphasic allometry. Wheeler’smodel would be considered valid if differentmeasures in different species satisfied theprediction, because the model is based on theevolution of a syndrome (i.e., the evolutionof a number of different characters that areexpected to change in loose synchrony). Tointerpret the current data, we need to reducethe details of our analysis to compose syn-dromes so that the broad patterns of evolu-tion are not lost in the metric details. Table1 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 thediscussion of fig. 5, and above) permits us to


Fig. 6. Caste syndromes defined by data of table 1 and ovarian dissection, optimized on cladogramof Wenzel and Carpenter. Where genera are polymorphic for caste syndrome, terminals are coded ac-cording to parsimonious optimization.

reformulate Richards’ syndromes and addone more. We propose the following groups:(1) casteless (no size or shape difference as-sociated with reproduction, females of allovarian conditions present); (2) physiologicalcaste only (no morphometric differences, butovarian condition unambiguous by absenceof type C females); (3) queens larger butmostly the same shape; (4) queens shapeddifferently with some measures smaller thanworkers. Although further research may findthis list (or characterization of given specieswithin the list) to be incomplete, we show

below that a powerful and coherent patternemerges from this perspective.

Figure 6 represents the working cladogramto date for Epiponini, from the cladogram ofWenzel and Carpenter (1994), rooted to a hy-pothetical ancestor that is without morpho-logical caste (Polistes, Mischocyttarus, etc.).Generic synonymies published since 1994have been incorporated here (Clypearia 5Occipitalia, Carpenter et al., 1996; Polybia5 Synoecoides, Carpenter et al., 2000; Lei-pomeles 5 Marimbonda, Carpenter, inpress). The original cladogram was reported


from analysis of Carpenter’s (1991) morpho-logical matrix of 31 characters (including afew traditional behavioral characters) andfrom Wenzel’s (1993) matrix of 21 behav-ioral or nest architectural characters, notoverlapping with those of Carpenter. None ofthe matrix characters included informationabout caste. The relevant caste syndromes, asdefined above, are plotted on the cladogramand optimized parsimoniously to hypotheti-cal ancestors. While figure 5 suggests a sprayof points in a continuum, the historical lin-eages are marked rather neatly in blocks infigure 6. The Epiponini in general is char-acterized as primitively casteless. Retainingthis primitive absence of caste, Angiopolybiapallens, Pseudopolybia vespiceps, Parachar-tergus fraternus, P. smithii, Leipomeles dor-sata, Chartergellus communis, and Nectari-nella championi all have high Wilks’ lambdavalue and poor queen–worker distinction(fig. 5). Without clear morphological caste,Synoeca, Clypearia, Asteloeca, and Metapo-lybia aztecoides have distinct physiologicaldifferences (but notice morphological varia-tion in M. docilis, fig. 5). This is the syn-drome we have added to Richards’ three, andif it were simply synonymized with ‘‘no mor-phological difference’’ then the absence ofcaste is even more definitively shown to bethe ancestral condition for Epiponini. SomePolybia and related genera have queens larg-er, and a few species of Polybia have queenswith some dimensions smaller, the final syn-drome. This last syndrome is also found inApoica (table 1). Agelaia vicina, Ag. palli-pes, Ag. multipicta, and other species in theliterature (table 1) also have developedqueens of different shape.

The most conspicuous feature of figure 6is that the interpretation of caste is rathersimple. Interestingly, the syndromes as de-fined by morphological and physiologicaldistinctions map rather neatly to traditionalgroups as recognized by gross nest architec-ture. At the foundation are the genera thathave covered nests and brood combs sup-ported by pedicels (‘‘calyptodomous, stelo-cyttarus’’ Richards, 1978; Wenzel, 1993; An-giopolybia to Nectarinella). The genera thatbuild with cells directly on the substrate(Synoeca to Asteloeca, the ‘‘astelocyttarus’’design of Richards) have physiological caste

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 andcombined with the matrices of Carpenter(1991) and Wenzel (1993), then differenttrees result. Figure 7 shows the principal dif-ference, which is that Apoica and Agelaia be-come sisters in a lineage basal to the remain-der of Epiponini. This is because the shapedifference of queens is enough to unite them,and it constitutes a more parsimonious plot,with only two derivations of queens smallerin some measure than workers, one in theApoica-Agelaia lineage and one in Polybialiliacea 1 Po. dimidiata. Future research willtest if Apoica and Agelaia are actually sisters.It seems that different models offered byWheeler (1991) and Jeanne et al. (1995) areboth fulfilled in different parts of the clado-gram, and that one syndrome has not beenaccounted for in previous models. The pro-posal from Jeanne et al. (1995) is fulfilled inthat Apoica derived queens of different shapewithout first developing different size, eitheralone (fig. 6) or with its sister Agelaia (fig.7), which may have derived size differencesindependently.

Wheeler’s (1991) more extensive model isfairly direct and general. Our explanation isderived simply from hers. Wheeler startedwith monophasic variation, meaning that thesame allometric relationships operate acrossa continuous spread of sizes (fig. 8A). Onecan imagine that the first step to distinctcastes is that the continuity in size is inter-rupted, producing individuals that differ insize and perhaps in behavioral role (fig. 8B).Once this distinction becomes regular, then itwould be easy to select for developmentalswitches that create different allometric re-lationships in the two size classes, meaningthat 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 isimproved by operating earlier in develop-ment, final gross body size may become ir-relevant, and castes could be produced suchthat they differ in morphology but not in size(fig. 8D). Such switches are already knownin Apis, where the fate of a larva is deter-mined early, and final body size is not causal


Fig. 7. Caste syndromes defined as in fig. 6, optimized on cladogram produced by using castesyndrome 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, representingmorphometric variation measured within a colony. See text for explanation.


to caste determination (Evans and Wheeler,1999). The presence of the predicted devel-opmental switch in Apis is encouraging, butthe best corroboration of the model would beto 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 exactlythis opportunity. Tracing along the bottom-most lineage, which subtends the major pathof genus-level diversity, demonstrates that insocial wasps there does appear to be stepwisedevelopment of the sort necessary to corrob-orate the model. Casteless societies give riseto those that differ in size, which give rise tothose that differ in shape, and some of theseinclude queens that are smaller (hence, a dis-sociation of size and morphological identity).Thus, the patterns we describe here includethe predictions of Wheeler’s model, evenconsidering the necessary placement of in-termediate states. We think that this is thefirst empirical validation of Wheeler’s modelto date.

Neither models by Jeanne et al. (1995) norWheeler (1991) anticipated the discovery of‘‘physiological caste only’’ as reported here,a group where ovary development is clear,with no persistent intermediates. The cladethat includes Synoeca and Asteloeca (fig. 6)has rather distinct reproductives upon dissec-tion, but discrimination is weak based on ourmeasures. These results are difficult to inter-pret, but the cladistic coherence of the syn-drome suggests that it is not an artifact. Topropose 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 amongmeasures from different colonies in differentgenera in different studies; that it is acciden-tal that only these species were united despitea field of other possibilities; that it is acci-dental that these species all fall out in a cla-distically interpretable pattern; and accidentalthat this pattern matches that of the tradition-al ‘‘astelocyttarus’’ nest architecture (seeWenzel [1991, 1993, 1998] for discussion ofnest form). The physiological switch that de-termines reproductivity in this group is notyet understood, but ‘‘cyclical oligogyny’’was discovered in this group and may pro-vide a key. West Eberhard (1978) reported

that queen number in Metapolybia is reducedin part through workers challenging queens,and this may eliminate intermediate femalesas well if the selection criterion is based onan estimate of fecundity. As such, queen se-lection by workers would seem to representan important social behavior that producesselection pressure to have an abrupt switchfrom nonreproductive to reproductive, and inthis clade it is separate from considerationsof size or shape, unlike Polybia and otherderived genera. Organization of labor in Me-tapolybia is also known to differ from thatof Polybia, being more simple (Karsai andWenzel, 1998; cf. Jeanne, 1986), and perhapsthis ‘‘astelocyttarus’’ clade has been over-looked for important transitional forms inother ways as well.

CONCLUSIONS

This analysis indicates that caste hasevolved 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 independentlines of argument. The first argument is thatfemales do not differ meaningfully either inmorphology or physiology. The second isthat the reproductives do not represent dom-inant animals, as they do in more primitivesocieties such as those of Polistes and Mis-chocyttarus. As discussed above, workers areknown 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 Angiopolybiathrough Nectarinella, and Synoeca throughAsteloeca do not represent the same socialrole as egglayers in Polistes; instead, they aresimply individuals that lay eggs in a societyof females that are not otherwise distin-guished. This may not have been recognizedbefore because, despite universal acceptanceof Hamiltonian perspectives regarding inclu-sive fitness, the community of vespid re-searchers still imagines wasps engaged in astruggle for direct fitness rather than joinedin a society of inclusive fitness. It seems like-ly that different types of socio-regulation ex-ist in epiponines as suggested by Noll andZucchi (2002). It is possible that some con-


fusion results in the literature from a desireto find a single syndrome to be representativeof the entire diversity of swarming wasps,whereas the actual evolution of caste has per-haps been multifaceted.

ACKNOWLEDGMENTS

We thank Jim Carpenter for suggestions onthe manuscript, Sidnei Mateus for his un-selfish expertise in fieldtrips and friendship,the OSU Social Insects Discussion Group forcommentary, and financial support fromOSU Research Foundation, Fapesp (Funda-cao de Amparo a Pesquisa do Estado de SaoPaulo) grant no. 01-02491-4 and CNPq.

REFERENCES

Baio, M.V., F.B. Noll, R. Zucchi, and D. Simoes.1998. Non-allometric caste differences in Age-laia vicina (Hymenoptera, Vespidae, Epiponi-ni). Sociobiology 34: 465–476.

Baio, M.V., F.B. Noll, and R. Zucchi. 2003a.Shape differences rather than size differencesbetween castes in the Neotropical swarm-founding wasp Metapolybia docilis (Hymenop-tera: Vespidae, Epiponini). BMC EvolutionaryBiology 3: 10.

Baio, M.V., F.B. Noll, and R. Zucchi. 2003b. Mor-phological caste differences, variation accord-ing to colony cycle, and non-sterility of work-ers in Brachygastra augusti (Hymenoptera,Vespidae, Epiponini), a Neotropical swarm-founding wasp. Journal of the New York En-tomological Society 111(4): 243–253.

Bourke, A.F.G. 1999. Colony size, social com-plexity and reproductive conflict in social in-sects. Journal of Evolutionary Biology 12:245–247.

Carpenter, J.M. 1991. Phylogenetic relationshipsand the origin of social behavior in the Vespi-dae. In K. G. Ross and R. W. Matthews (edi-tors), The social biology of wasps: 7–32. Itha-ca, NY: Cornell University Press.

Carpenter J.M. 1993. Biogeographic patterns inthe Vespidae (Hymenoptera): Two views of Af-rica and South America. In P. Goldblatt (editor),Biological relationships between Africa andSouth America, pp. 139–155. New Haven, CT:Yale University Press, ix 1 630 pp.

Carpenter, J.M. 1997. A note on the names of pa-per wasp tribes (Insecta: Hymenoptera: Vespi-dae). Ibaraki University Natural History Bul-letin 1: 15–16.

Carpenter, J.M. (in press). Synonymy of the genusMarimbonda Richards, 1978, with Leipomeles

Mobius, 1856 (Hymenoptera: Vespidae; Polis-tinae), and a new key to the genera of paperwasps of the New World. American MuseumNovitates.

Carpenter, J.M., J.I. Kojima, and J.W. Wenzel.2000. Polybia, paraphyly, and polistine phylog-eny. American Museum Novitates 3298: 24 pp.

Carpenter, J.M., and K.G. Ross. 1984. Colonycomposition in four special of Polistinae fromSuriname, with a description of the larva ofBrachygastra scutellaris (Hymenoptera, Ves-pidae). Psyche 91: 237–250.

Carpenter, J.M., J.W. Wenzel, and J. Kojima.1996. Synonymy of the genus Occipitalia Rich-ards, 1978, with Clypearia de Saussure 1854(Hymenoptera: Vespidae; Polistinae, Epiponi-ni). Journal of Hymenoptera Research 5: 157–165.

Evans, H.E., and M.J. West-Eberhard. 1970. Thewasps. Ann Arbor, MI: University of MichiganPress, vii 1 265 pp.

Evans, J.D., and D.E. Wheeler. 1999. Differentialgene expression between developing queensand workers in the honey bee, Apis mellifera.Proceedings of the National Academy of Sci-ences, USA 96: 5575–5580.

Gadagkar, R. 1987. Social structure and the de-terminants of queen status in the primitively eu-social wasp Ropalidia cyanthiformis. IUSSI,Munchen, 377–378.

Gadagkar, R., and N.V. Joshi. 1982. A compara-tive study of social structure in colonies of Ro-palidia. IX Congr. IUSSI, Boulder, Colorado,187–191.

Gadagkar, R., and N.V. Joshi. 1983. Quantitativeethology of social wasps: Time activity budgetsand caste differentiation in Ropalidia marginata(Hymenoptera, Vespidae). Amimal Behaviour31: 26–31.

Hebling, N.J., and V.L.G. Letızio. 1973. Polimor-fismo de las castas femininas de Polybia ema-ciata. Boletim da Sociedade Entomolgica doBrasil 7(1): 23–24.

Hunt J.H. 1999. Trait mapping and salience in theevolution of eusocial vespid wasps. Evolution53(1): 225–237.

Hunt J.H., S. O’Donnell, N. Chernoff, and C.Brownie. 2001. Observations on two neotropi-cal swarm-founding wasps, Agelaia yepocapaand A. panamaensis (Hymenoptera: Vespidae).Annals of the Entomological Society of Amer-ica 94: 555–562.

Hunt J.H., D.K. Schmidt, S.S. Mulkey, and M.A.Williams. 1996. Caste dimorphism in Epiponaguerini (Hymenoptera: Vespidae): Further evi-dence for larval determination. Journal of Kan-sas Entomological Society 69(4): 362–369.

Ito, Y. 1986. On the pleometrotic route of social


evolution in the Vespidae. Monitore ZoologicoItaliano 20: 241–262.

Jeanne, R.L. 1980. Evolution of social behaviorin the Vespidae. Annual Review of Entomology25: 371–395.

Jeanne, R.L. 1986. The organization of work inPolybia occidentalis: the costs and benefits ofspecialization in a social wasp. BehavioralEcology and Sociobiology 19: 333–341.

Jeanne R.L. 1991. The swarm–founding Polisti-nae. In K. G. Ross and R. W. Matthews (edi-tors), The Social Biology of Wasps: 191–231.Ithaca, NY: Cornell University Press.

Jeanne R.L. 1996. Non-allometric queen-workerdimorphism in Pseudopolybia difficilis (Hy-menoptera: Vespidae). Journal of Kansas En-tomological Society 69(4): 370–374.

Jeanne R.L., and R. Fagen 1974. Polymorphismin Stelopolybia areata (Hymenoptera, Vespi-dae). Psyche 81: 155–166.

Jeanne, R.L., C.A. Graf, and B.S. Yandell. 1995.Non-Size-Based morphological castes in a so-cial insect. Naturwissenschaften 82: 296–298.

Karsai, I., and J.W. Wenzel. 1998. Productivity,individual-level and colony-level flexibility, or-ganization of work as a consequence of colonysize. Proceedings of the National Academy ofSciences, USA 95: 8665–8669.

Keeping, M.G. 2000. Morpho-physiological vari-ability and differentiation of reproductive rolesamong foundresses of the primitively eusocialwasp, Belonogaster petiolata (Degeer) (Hyme-noptera, Vespidae). Insectes Sociaux 47(2):147–154.

Keeping, M.G. 2002. Reproductive and workercastes in the primitively eusocial wasp Belon-ogaster petiolata (DeGeer) (Hymenoptera: Ves-pidae): evidence for pre-imaginal differentia-tion. Journal of insect physiology 48(9): 867–879.

Kukuk, P.F. 1994. Replacing the terms ‘primitive’and ‘advanced’: new modifiers for the term ‘eu-social’. Animal Behavior 47: 1475–1478.

Mateus, S., F.B. Noll, and R. Zucchi. 1997. Mor-phological caste differences in neotropicalswarm-founding polistinae wasps: Parachar-tergus smithii (Hymenoptera: Vespidae). Jour-nal of the New York Entomological Society105(3–4): 129–139.

Mateus, S., F.B. Noll, and R. Zucchi. 1999. Castedifferences and related bionomic aspects ofChartergellus communis, a neotropical swarm-founding polistine wasp (Hymenoptera: Vespi-dae: Polistinae: Epiponini). Journal of the NewYork Entomological Society 107(4): 390–405.

Mateus, S., F.B. Noll, and R. Zucchi. 2004. Casteflexibility and variation according to the colonycycle in the swarm-founding wasp, Parachar-

tergus fraternus (Hymenoptera: Vespidae: Epi-ponini). Journal Kansas Entomological Society77(4): 281–294.

Maule-Rodrigues, V., and B.B. Santos. 1974. Ves-pıdeos sociais: Estudo de uma colonia de Po-lybia dimidiata (Olivier, 1791) (Hymenoptera,Polistinae). Rev. bras. Ent., 18(2): 37–42.

Naumann, M.G. 1970. The nesting behavior ofProtopolybia pumila (Saussure, 1863) (Hyme-noptera: Vespidae) in Panama. Doctoral Disser-tation, University of Kansas, Kansas.

Noda, S.C.M., S.N. Shima, and F.B. Noll. 2003.Morphological and physiological caste differ-ences in Synoeca cyanea (Hymenoptera, Ves-pidae, Epiponini) according to the ontogeneticdevelopment of the colonies. Sociobiology 41:547–570.

Noll, F.B., S. Mateus, and R. Zucchi. 1996. Mor-phological caste differences in neotropicalswarm-founding Polistinae wasps V: Protopo-lybia exigua exigua (Hymenoptera, Vespidae).Journal of the New York Entomological Soci-ety 104: 62–69.

Noll, F.B., D. Simoes, and R. Zucchi 1997. Mor-phological caste differences in neotropicalswarm-founding polistinae wasps. Agelaia m.multipicta and A. p. pallipes (Hymenoptera:Vespidae). Ethology, Ecology and Evolution 9:361–372.

Noll F.B., S. Yamane, and R. Zucchi. 2000. Mor-phological caste differences in the Neotropicalswarm-founding polistine wasps. IX. Polybia(Myrapetra) occidentalis (Hymenoptera, Ves-pidae). Entomological Sciences 3(3): 491–497.

Noll, F.B., and R. Zucchi. 2000. Increasing castedifferences related to life cycle progression insome neotropical swarm-founding polygynicwasps (Hymenoptera: Vespidae: Epiponini).Ethology, Ecology and Evolution 12(1): 43–65.

Noll F.B., and Zucchi R. 2002. Castes and theinfluence of the colony cycle in swarm-found-ing polistine wasps (Hymenoptera: Vespidae;Epiponini). Insectes Sociaux 49: 62–74.

O’Donnell, S. 1998. Reproductive caste determi-nation in eusocial wasps (Hymenoptera: Ves-pidae). Annual Review of Entomology 43:323–346.

Oster, G.F., and E.O. Wilson. 1978. Caste andecology in the social insects. Monographs inpopulation biology. Princeton University Press,352 pp.

Pardi, L., and M.T.M. Piccioli. 1981. Studies onthe biology of Belonogaster (HymenopteraVespidae). 4. On caste differences in Belono-gaster griseus (Fab.) and the position of thisgenus among social wasps. Monitore ZoologicoItaliano, n. ser., Supplemento XIV, 9: 131–146.

Pickett, K.M. 2003. Evolution of transitional


forms: behavior, colony dynamics, and phylo-genetics of social wasps (Hymenoptera: Ves-pidae). Ph.D. dissertation, The Ohio State Uni-versity, Columbus, Ohio.

Reeve, H.K. 1991. Polistes. In K.G. Ross andR.W. Matthews (editors), The social biology ofwasps: 99–148. Ithaca, NY: Cornell UniversityPress.

Richards, O.W. 1978. The Social Wasps of theAmericas, Excluding the Vespinae. London:British Museum (Natural History).

Richards, O.W., and M.J. Richards. 1951. Obser-vations on the social wasps of South America(Hymenoptera, Vespidae). Transactions of theRoyal Entomological Society of London 102:1–170.

Sakagami, S.F., R. Zucchi, S. Yamane, F.B. Noll,and J.M.F. Camargo. 1996. Morphological castedifferences in Agelaia vicina, the neotropicalswarm-founding polistine wasp with the largestcolony size among social wasps (Hymenoptera:Vespidae). Sociobiology 28(2): 207–223.

Shima S.N., F.B. Noll, and R. Zucchi. 2000. Mor-phological caste differences in the neotropicalswarm-founding polistine wasp, Brachygastralecheguana (Hymenoptera: Vespidae, Polisti-nae, Epiponini). Sociobiology 36(1): 41–52.

Shima S.N., F.B. Noll, and R. Zucchi. 2003. In-fluence of the colony cycle on physiologicaland morphological caste variation in the peren-nial neotropical swarm-founding social wasp,Protonectarina sylveirae (Hymenoptera, Ves-pidae, Epiponini). Sociobiology 42(2): 449–466.

Shima S.N., F.B. Noll, R. Zucchi, and S. Yamane1998. Morphological caste differences in theneotropical swarm-founding polistine wasps IV.Pseudopolybia vespiceps, with preliminaryconsiderations on the role of intermediate fe-males in social organization of the Epiponini(Hymenoptera, Vespidae). Journal of Hyme-noptera Research 7: 280–295.

Shima S.N., S. Yamane, and R. Zucchi. 1994.Morphological Caste Differences in Some neo-tropical Swarm-founding polistine wasps I.Apoica flavissima (Hymenoptera, Vespidae).Japanese Journal of Entomology 62(4): 811–822.

Shima S.N., S. Yamane, and R. Zucchi. 1996a.Morphological caste differences in some neo-tropical swarm-founding polistine wasps II. Po-lybia dimidiata (Hymenoptera, Vespidae). Jap-anese Journal of Entomology 64(1): 131–144.

Shima S.N., S. Yamane, and R. Zucchi. 1996b.Morphological caste differences in some neo-tropical swarm-founding polistine wasps III.Protonectarina sylveirae (Hymenoptera, Ves-

pidae). Ibaraki University Bulletin of the Fac-ulty of Education, 45: 57–67.

Simoes, D. 1977. Ethology and caste differentia-tion in some social wasps (Hymenoptera; Ves-pidae). Ph.D. dissertation, Universidade de SaoPaulo; Ribeirao Preto, Sao Paulo, 182 pp.

Spradbery, J.P. 1991. Evolution of queen numberand queen control. In K. G. Ross and R. W.Matthews (editors), The social biology ofwasps: 336–388. Ithaca, NY: Cornell Univer-sity Press.

Strassmann, J.E., D.C. Queller, C.R. Solis, andC.R. Hughes. 1991. Relatedness and queennumber in the neotropical wasp, Paracharter-gus colobopterus. Animal Behaviour 42: 461–470.

Strassmann J.E., B.W. Sullender, and D.C. Quell-er. 2002. Caste totipotency and conflict in alarge-colony social insect. Proceedings of theRoyal Society of London Series B, BiologicalSciences 269(1488): 263–270.

Turillazzi S. 1991. The Stenogastrinae. In K. G.Ross and R. W. Matthews (editors), The socialbiology of wasps: 74–98. Ithaca, NY: CornellUniversity Press.

Turillazzi S., E. Francescato, A.B. Tosi, and J.M.Carpenter. 1994. A distinct caste difference inPolybioides tabidus (Fabricius) (Hymenoptera,Vespidae). Insectes Sociaux 41(3): 327–330.

Wenzel, J.W. 1992. Extreme queen-worker di-morphism in Ropalidia ignobilis, a small-col-ony wasp (Hymenoptera: Vespidae). InsectesSociaux 39: 31–43.

Wenzel, J.W. 1993. Application of the biogeneticlaw to behavioral ontogeny: a test using nestarchitecture in paper wasps. Journal Evolution-ary Biology 6: 229–247.

Wenzel, J.W. 1991. The evolution of nest archi-tecture in the social vespids. In K.G. Ross andR.W. Matthews (editors), The social biology ofwasps: 480–519. Ithaca, NY: Cornell Univer-sity Press.

Wenzel, J.W. 1998. A generic key to the nests ofhornets, yellowjackets, and paper wasps world-wide (Vespidae: Vespinae, Polistinae). Ameri-can Museum Novitates 3224: 1–39.

Wenzel, J.W., and J.M. Carpenter. 1994. Compar-ing methods: adaptive traits and tests of adap-tation. In P. Eggleton and R. I. Vane-Wright(editors), Phylogenetics and ecology: 79–101.London: Academic Press.

West-Eberhard, M.J. 1978. Temporary queens inMetapolybia wasps: non-reproductive helperswithout altruism? Science 200: 441–443.

West-Eberhard, M.J. 1981. Intragroup selectionand the evolution of insect societies. In R.D.Alexander and D.W. Tinkle (editors), Natural


selection and social behavior, pp. 3–17. NewYork: Chiron Press.

West-Eberhard, M.J. 1996. Wasp societies as mi-crocosms for the study of development andevolution. In S. Turillazzi and M.J. West-Eber-hard (editors), Natural history and evolution ofpaper-wasps: 290–317. Oxford UniversityPress.

Wheeler, D.E. 1991. The developmental basis ofworker castes polymorphism in ants. AmericanNaturalist 138: 1218–1238.

Wilson, E.O. 1985. The sociogenesis of insectcolonies. Science 228(4704): 1479–1485.

Yamane, S., J. Kojima, and S.K. Yamane. 1983.Queen/worker size dimorphism in an Oriental

polistine wasp, Ropalidia montana Carl (Hy-menoptera, Vespidae). Insectes Sociaux 30:416–422.

Yamane, S., and Y. Maeta. 1985. Notes on thehibernation of Parapolybia indica (Hymenop-tera, Vespidae). Kontyu 53: 576–577.

Yamane, S., and Y. Ito. 1987. Caste differentiationand social organization in the Old World Ves-pidae. IUSSI, Munchen, 265–266.

Zucchi, R., S.F. Sakagami, F.B. Noll, M.R. Mechi,M.V. Baio, S. Mateus, and S.N. Shima. 1995.Agelaia vicina, a swarm-founding Polistinaewith the largest colony size among wasps andbees (Hymenoptera, Vespidae). Journal of theNew York Entomological Society 103(2): 129–137.

Recent issues of the Novitates may be purchased from the Museum. Lists of back issues of theNovitates and Bulletin published during the last five years are available at World Wide Web sitehttp://library.amnh.org. Or address mail orders to: American Museum of Natural History Library,Central Park West at 79th St., New York, NY 10024. TEL: (212) 769-5545. FAX: (212) 769-5009. E-MAIL: [email protected]

a This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

Documents

Evolution of Caste in Neotropical Swarm Founding Wasps (Hymenoptera: Vespidae; Epiponini): 10 Tables