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The continuum ing can be regarded as eusocial, just as eu- social are cooperative breeders. We believe Pud W. Sherman this integrated approach will foster potentially revealing Section of Ncurobiology and , cross-taxon comparisons, which are essential to under- Cornell University, standing social in , , and in- Ithaca, NY 14853. USA sects. Key words: avion eusociality, cooperative breed- ing, eusociality, mammalian eusociality, reproductive Eileen A. Lacey skews, social system convergence. [Behav Ecol 6:102- Behavior Croup, 108 (1995)] University of California, Davis, CA 95616. USA The has been an important Hudson K. Reeve puzzle ever since Darwin (1859: 268) identified Section of Neurobiology and Behavior, worker as presenting "one special difficulty, Cornell University, which at first appeared to me insuperable, and ac- Ithaca, NY 14853, USA tually fatal to the whole theory." In 1966, Batra coined the term eusocial (meaning truly social) to Laurent Keller Zoological Institute, describe halictine in which "the founding Bern University, parent survives to cooperate with a group of her Ethologische Station Hasli, mature daughters, with division of labor" (p. 375). CH-3052 Hinterkappelen, Subsequently, Michener (1969: 305) referred to Switzerland bees as eusocial if they lived in "matrifilial and groups consisting of.. . mothers and daughters. .. Institute of and Animal , [showing] division of labor with more or less rec- University of Lausanne, ognizable castes (egg layers and workers)." Bitiment de Biologic, In 1971, Wilson broadened these criteria to in- CH-I0I5 Lausanne, Switzerland clude other . Following his lead, Holldobler and Wilson (1990: 638) denned eusocial as those exhibiting " in caring for the Eusocial are traditionally characterized by a young; reproductive division of labor, with more reproductive division of labor, an overlap of generations, or less sterile individuals working on behalf of in- and cooperative care of the breeders' young. Eusociality dividuals engaged in ; and overlap of was once thought to occur only in , ants, and at least two generations of life stages capable of some and species, but striking evolutionary contributing to labor." Once thought to convergences have recently become apparent between the occur only in the orders (ants, bees, societies of these insects and those of cooperatively breed- and ) and Isoptera (termites), eusociality has ing birds and mammals. These parallels have blurred now been reported in Japanese (Homop- distinctions between and eusocial- tera: Aoki, 1982; I to, 1989), Australian (Co- ity, leading to calls for either drastically restricting or leoptera: Kent and Simpson, 1992), Australian expanding usage of these terms. We favor the latter (Thysanoptera: Crespi, 1992), and African approach. Cooperative breeding and eusociality are not mole-rats (Rodentia: Burda and Kawalika, 1993; discrete phenomena, but rather form a continuum of Jarvis and Bennett, 1993;JarvisetaI., 1991,1994). fundamentally similar social systems whose main dif- As detailed information has accumulated on the ferences lie in the distribution of lifetime reproductive reproductive and of vertebrates and success among group members. Therefore we propose to invertebrates, distinctions between eusociality and array and cooperative breeders other social systems have become blurred. Indeed, along a common axis, representing a standardized mea- a number of authors have identified striking evo- sure of reproductive variance, and to drop such (loaded) lutionary parallels between the social systems of terms as "primitive" and "advanced" eusociality. The cooperatively breeding birds and mammals and terminology we propose unites all occurrences of olio- those of social insects (e.g., Alexander etal., 1991; parental helping of kin under a single theoretical um- Andersson, 1984; Emlen et al., 1991; Lacey and brella (e.g., Hamilton's rule). Thus, cooperatively breed- Sherman, 1991; Reeve and Sherman, 1991; Veh-

102 Vol. 6 No. 1 rencamp, 1979). Further, as Seger (1991: 346) not- the distinguishing attributes (e.g., morphological ed, detailed studies of insects have revealed a broad differentiation of colony members) is continuous, spectrum of social organizations among species tra- rather than discrete, both widiin and among taxa. ditionally characterized as eusocial (e.g., see Keller, Finally, the terms "primitive" and "advanced" are 1993; Michener, 1985; Ross and Matthews, 1991). both value-laden and ambiguous, as they may refer Not surprisingly, therefore, several authors (e.g., either to social complexity (sensu Michener, 1969) Crespi and Yanega, 1994; Tsuji, 1992) have re- or similarity to presumed ancestral forms (sensu cently questioned the adequacy of traditional def- Carpenter, 1991). initions of eusociality. Problems have arisen pri- To resolve these ambiguities, we propose using marily because the key denning characteristic— variation in lifetime reproductive success (LRS) "reproductive division of labor, with more or less among members of cooperatively breeding social sterile individuals working"—is vague and thus am- groups to quantify "reproductive division of la- biguous in its application. One solution is to define bor." Reproductive differences are central to all eusociality more narrowly. This approach has been definitions of eusociality, and they underlie much adopted by Tsuji (1992) and Crespi and Yanega of die diversity among vertebrate and invertebrate (1994), who argue that the term should be applied societies (see Bourke, 1991; Vehrencamp, 1979). to only a subset of the insects currendy recognized Such differences result from social competition and as eusocial. Alternatively, definitional problems suppression within groups as well as ecological fac- could be reduced by expanding the eusociality con- tors that preclude reproduction by some group cept to include all vertebrate and invertebrate so- members. Differences in LRS provide an evolu- cieties with helpers. tionarih/ relevant basis for interspecific compari- We favor the latter approach. It seems more pro- sons because it is through such differences that ductive to recognize that similar social systems oc- shapes the morphology, physiol- cur in birds, mammals, and insects than to debate ogy, and behavior of eusocial species. whedier particular insects are eusocial (e.g., Furey, One could standardize LRS variation in numer- 1992 versus Tsuji, 1992). Behavioral convergences ous ways. One possibility is the index of reproduc- between eusocial insects and cooperatively breed- tive skew (5) developed by Reeve and Ratnieks ing vertebrates should long ago have focused our (1993) and Keller and Vargo (1993): attention on common selective factors favoring so- ciality and alloparental care in these taxa (see Strassmann and Queller, 1989). Research on these N> + N. groups has proceeded largely independently, how- where Nm is the number of nonbreeding alloparents ever, and as a result there is currendy one set of (helpers) in a group, Nt is the number of breeders evolutionary explanations for cooperative breeding in the group (some of which may also behave as in birds and mammals (e.g.. Brown, 1987; Emlen, alloparents), and v is a measure of the variation in 1991; Jennions and Macdonald, 1994) and a par- reproductive success among breeders. In groups allel, but distinct, set of explanations for containing a single breeder, v is defined as 1.0; in in insects (e.g., Seger, 1991; Trivers, 1985). We groups widi multiple breeders, v is the variance suggest that the evolution of sociality in both groups among breeders in their proportion of die summed will be best understood if these explanations are LRS of the group divided by the maximum possible merged. value for diis variance. Thus, v — N^s*, where J1 is As a first step toward this unification it would be the sample variance in die proportion of total off- useful to have a quantitative way to compare social spring produced by breeders: systems across diverse taxa. Current schemes for comparing societies are qualitative, however, and emphasize traits that result only secondarily from reproductive differences among colony mem- bers. For example, some authors (e.g., Cowan, 1991; (N»- 1) Eickwort, 1981; Michener, 1974) distinguish "ad- (in diis expression, p, is die proportion of offspring vanced" from "primitive" eusociality. Advanced produced by die idi breeder). eusocial species inhabit large, long-lived colonies Using S, one can begin to compare die degree containing worker* that typically are unable to mate of reproductive skew widiin and among social spe- and that are well-differentiated morphologically cies on a common scale diat ranges from 0 to 1. from queens, whereas primitively eusocial species When LRS is equal among group members, S — 0; live in small, often annual colonies containing work- when reproduction is restricted to a single individ- ers that are morphologically similar to queens and, ual and odier group members never breed, S =• 1. usually, capable of . If, as seems likely, skews vary considerably among The advanced-primitive dichotomy was erected conspecific groups or populations, dien species may primarily to categorize morphological and social be represented as segments of die scale radier dian complexity, not unevenness in reproduction. As a as points. The index of reproductive skew can be result it only crudely discriminates between soci- calculated for males only, females only, or bodi eties with weakly versus sharply defined reproduc- sexes, depending on who participates in allopar- tive divisions of labor. For example, worker repro- ental care—e.g., females in species of social Hy- duction occurs in many "advanced" eusocial ants menoptera, males in many cooperatively breeding (Bourke, 1988; Choc, 1988) but not in queenright birds, and both sexes in termites and some carni- colonies of some "primitively" eusocial bees (Mich- vores. ener et al., 1979) and wasps (reviewed by Reeve, We emphasize dial die S index of Reeve and 1991). Moreover, diis dichotomy is difficult to ap- Ratnieks (1993) and Keller and Vargo (1993) is ply to specific cases because variation in each of used for illustrative purposes, as one possible way

Forum 103 include Florida scrub jays (Aphelcoma coerulescens: The Eusociality Continuum Fitzpatrick and Woolfenden, 1988; Woolfenden and Fitzpatrick, 1984), splendid fairy-wrens (Malurus splendtns: Rowley and Russell, 1990), stripe-backed Index of Reproductive Skew wrens (Campjlorhjnchus nuchalis: Rabenold, 1990), green woodhoopoes (Phoeniculus purpureus: Ugon and Ligon, 1990), golden (Cants aureus: Moehlman, 1986), pine (Microius pirutorum: B FitzGerald and Madison, 1983; Powell and Fried, 1992), and certain marmosets (Sagutnvs spp.: Groove- Florida Dwarf Fungus Snowdon and Soini, 1988), tamarins (Callithrix spp.: billed AnJs Scrub Jays Mongooses Ants Stevenson and Ryiands, 1988), stenogastrine wasps lAtta) Acorn Stripe-backed Naked (Turillazzi, 1991), carpenter bees (Hogendoorn and Wrens Mole-Rats Yellow- Vdthuis, 1993; Stark, 1992), and social (e.g., lacket Anelosimus extmhis: Rypstra, 1993; Vollrath, 1986). Black-tailed Golden African Wild Dogs Wasps Prairie Dogs Jackals () Toward the middle of the scale (subinterval B in Hallctld Spotted Stcnogas trine Bees Mound- Figure 1) wul be singular breeding societies in which Hyenas Wasps (AitgoctxkjreOjCi building opportunities for direct reproduction by helpers tPariachnogaster strtataj Termites are limited throughout life. In these cases, helping nigrlcans) (Maavtermes) is not simply an ontogenetic stage through which Paper Carpenter Bees Wasps Pemphlgld most or all individuals pass prior to reproducing OCytocopa Aphlds directly. Instead, because of limited opportunities sulcatipes) (Pemphigus) Damp-wood for direct reproduction, only a fraction of helpers Social Spiders Termites Honey Bees in these species will eventually produce offspring, (AndosUrms (ApisJ usually via immigration to groups lacking a repro- ocbrdus} neuadensis) ductive or supersedure within groups. Examples include naked mole-rats {fieterocephalus glaber. Figure 1 to construct a continuum for eusociality (see also Sherman et al., 1991,1992), damaraland mole-rats Intervals within which the Bourke, 1991). S provides only a rough summary (Cryptomys damarensis: Jarvi* and Bennett, 1993; societies of selected vertebrate of the distribution of LRS among group members, Jarvis et al., 1994), dwarf mongooses (Helogale par- and invertebrate cooperative because different social groups with similar skew vtda: Creel and Waser, 1991; Rood, 1986), African breeders are expected to indices could have LRS distributions that differ in wild dogs (JLycaon pietur. Frame et al., 1979; Mal- occur on a common scale of shape (e.g., in other continuous parameters such colm and Marten, 1982), (Omis lupus: Har- intragroup skew in lifetime reproductive success (see the as skewness or kurtosis). Nonetheless, we suggest rington et al., 1983), some halictid bees (e.g., Au- text). There is no skew (Le., 0) that 5 provides a useful preliminary method for gochlorellastriata: Mueller, 1991; L. breedi: Michener when LRS U equal among identifying potentially similar social systems. et al., 1979; L. figutrtsi: Wcislo et al., 1993), paper members of a ; Although detailed data on LRS are not available wasps (e.g., fuscatur. Klahn, 1981; Metcalf, skew is maximal (i-e., 1) when for most social insects and cooperatively breeding 1980), small-colony termites (e.g., Incisitermts reproduction is restricted to a vertebrates, existing behavioral and demographic schwarzi: Luykx, 1993; Zootermopsis ntvadmsis: single individual of each sex information allows us to predict the relative posi- Shellman-Reeve, in press) and many per group and helpers never tions of different societies along a scale of skew in (Bombus spp.: Free and Butler, 1959). breed. When skews vary LRS. At the low end of the scale (in subinterval A Finally, at the upper end of the scale (subinterval considerably among consperific groups or of Figure 1), lie helper-at-the nest/den societies C in Figure 1) will be societies exhibiting consistent, populations, species are best with multiple reproductive individuals per group pronounced intragroup differences in LRS due to represented as line segments (e.g., "joint-nesting plural breeders," Brown, 1987). the virtual absence of direct reproduction by most denoting intraspecinc ranges. Examples of such societies include groove-billed group members. Familiar examples are social in- Indices of reproductive skew anis (Crotophaga sulrirostrir. Koford et al., 1990; sects with physiologically sterile or semi-sterile may be calculated for male Vehrencamp et al., 1988), acom woodpeckers (Afc- workers, such as Japanese aphids {Pemphigus spp.: group members only, females tanrrpes farmidvorouy. Koenigand Muramc, 1987), Benton and Foster, 1992; Foster, 1990; Ito, 1989), only, or both sexes, black-tailed prairie dogs (Cynomjs ludovicianus: fungus ants (Atta spp.: Holldobler and Wilson, depending on who Hoogiand, in press), spotted hyenas (Croatia cro- 1990), yellow-jacket wasps (Vespula and Dolichoves- participates in alloparental care; for this figure, only cuta: Frank, 1986; Frank et al., in press), pula spp.: Greene, 1991), large-colony termites female reproductive skews are (Panthera Uo: Packer et aL, 1988), and banded mon- (Macrotermes spp.: Wilson, 1971), and honeybees considered. For clarity of gooses (Mungas mungo: Rood, 1986). Polyandrous (Apis mellifera: Page and Metcalf, 1984). presentation, societies that cooperative breeders, in which male helpers mate Societies that lie at different positions along the apparently exhibit similar widi the breeding female (e.g., Arabian babblers, scale of reproductive skew differ in several ways. reproductive skews are Turdoides squamiceps: Zahavi, 1990), will also lie at Most importantly, those at the upper end live in grouped together, intervals A, the lower end of the scale, but exactly where de- larger groups, indeed usually orders of magnitude B, and C are not meant to pends on how unevenly paternity is divided among larger, than societies in the middle and at the lower denote separate categories in the attending males. the eusociality continuum. end of the scale. Group size has two important Societies in which auxiliaries do not reproduce evolutionary implications for the elaboration of al- while helping (i.e., "singular breeders," Brown, loparental care. First, as group size increases, the 1987) but have a reasonable probability of suc- probability decreases that a particular individual cessfully dispersing and producing offspring later will be able to fill any within-group breeding va- in life are also expected to fall toward the low end cancy (see Reeve and Ratnieks, 1993). Thus, in of the scale. Reproductive skews for these societies species that live in large groups, individuals may will likely be higher than those for joint-nesting transmit their genes more effectively by specializing plural breeders because of helper mortality while physiologically, morphologically, and/or behavior- behaving as alloparents. Examples of such societies ally to help relatives than they would by retaining

104 Behavioral Ecology Vol. 6 No. 1 the capacity to personally reproduce and either Some readers may balk at our attempt to broaden waiting for a breeder's demise or attempting to the concept of eusociality. Indeed, Crespi and reproduce in the breeder's presence. This is es- Yanega (1995) propose to resolve ambiguities in pecially true if retaining the capacity to reproduce the traditional definition by restricting eusociality diminishes a helper's effectiveness, or if alloparen- to societies with irreversibly behaviorally distinct tal care greatly enhances group reproductive out- groups (castes), one or more of which is not "to- put. Second, a positive relationship between group tipotent" (i.e., does not exhibit the full behavioral size and specialization of helper phenotypei can repertoire of the species). They further separate also arise due to severe ecological conditions that "facultatively eusocial" societies, in which only the strongly favor both the formation of large groups "more-reproductive" caste is totipotent, from "ob- and alloparental care of young. Under these cir- ligately eusocial" societies, in which neither caste cumstances, natal and helping relatives is totipotent. When there is reproductive division may so consistently yield the highest inclusive fit- of labor and altruistic alloparental care, but no ness payoffs that irreversible specializations for irreversible reduction in the behavioral repertoire helping evolve. of the alloparents, Crespi and Yanega term the For these reason* the inability to reproduce may "cooperatively breeding." Such societies are be obligate among large-colony societies, but fac- further subdivided into "quasisocial" and "semi- ultative among small-colony societies. Direct con- social," depending on whether the distribution of flict over reproduction is more characteristic of LRS is unimodal or bimodal. This classification sys- cooperative breeders that live in small groups (e.g., tem roughly maps out as ordered segments along wolves: Zimen, 1976; dwarf mongooses: Creel et the continuum in our Figure 1 (e.g., proceeding al., 1992; naked mole-rats: Faulkes et al., 1990; from the left, quasisocial cooperative breeding, paper wasps: Reeve and Nonacs, 1992; Reeve and semisocial cooperative breeding, facultative euso- Ratnieks, 1993) than those that live in very large ciality, and obligate eusociality). groups. The evolution of specialized helper phe- We have several reservations regarding Crespi notypes (e.g., castes) and intragroup breeding con- and Yanega's definitional scheme. First, it catego- flict thus are apparently related to group size, which rizes societies as eusocial using a phenotypic feature is itself a of the ecological advantages of ("irreversible behavioral distinctness") that is just group-living. one possible evolutionary outcome of reproductive Societies that lie at different positions along the differences among colony members. Crespi and scale of reproductive skew should also differ in the Yanega state that "loss of totipotency is probably distribution of LRS within social groups. Histo- the most cvolutionarily relevant event in social evo- grams of LRS for societies at the lower end will be lution, because it results in distinct, divergent, life- roughly unimodal and symmetric or slightly skewed. time behavioral trajectories." This justification is For societies more toward the middle, LRS will be insufficient, as it fails to indicate why lifetime dif- unimodal and strongly skewed, became some in- ferences in behavior are significant—simply stating dividuals produce many offspring but the majority that reductions in behavioral repertoires lead to produce only a few. At the upper end of the scale, increased behavioral specializations is not compel- histograms of LRS will be bimodal and lacking in ling. Although Crespi and Yanega go on to suggest intermediate classes: a few individuals produce all that loss of totipotency is important because selec- the young, whereas the rest do not reproduce (e.g., tion on the behavior of newly arisen castes "has for data on honeybees, see Page and Metcalf, 1984). become circumscribed," this argument confuses Bimodality is more evident at the high end of the ontogenetic reversibility with potential for selective scale because societies with extreme reproductive modification—concepts at two different logical lev- skews are mostly large-colony social insects in which els of analysis. maximum lifetime fecundity of queens versus work- Second, the Crespi-Yanega scheme effectively ers is far greater than that of female breeders versus restricts eusociality to invertebrates. The separa- helpers in cooperatively breeding vertebrate soci- tion of invertebrate from vertebrate societies tends eties. to decouple evolutionary explanations for euso- These considerations suggest that eusociality is ciality and cooperative breeding. This is unfortu- best viewed as a continuum rather than a discrete nate because vertebrate and invertebrate social sys- phenomenon. If eusociality is regarded as discrete, tems are not fundamentally different, but instead whatever "break point" on the scale of LRS skew vary quantitatively with respect to the same under- is chosen as the denning cut-off would be arbi- lying evolutionary principles (e.g., Hamilton's rule; trary. Using the same logic, Shields (1993) recently see Grafen, 1991). Under Crespi and Yanega's di- argued against arbitrarily dichotomizing inbreed- chotomous scheme, however, similar social systems, ing versus outbreeding: because genetic related- such as those of naked mole-rats and sweat bees, ness among mates is a continuous variable, inbreed- are conceptually segregated, whereas rather dissim- ing also is a continuum. Although skews in LRS for ilar social systems, such as those of dwarf mon- social insects will often be greater than those for gooses and social spiders, are lumped together. vertebrates, we expect these values to overlap, with Third, Crespi and Yanega place many societies no quantitative discontinuities between taxa. Given that have traditionally been recognized as eusocial that most cooperatively breeding birds and mam- (e.g., some paper wasps, hover wasps, halictid bees, mals already meet two of the three traditional cri- ponerine ants, and mole-rats; see Eickwort, 1986; teria for eusociality (overlap of generations and Jarvis, 1981; Peeters, 1993; Turillazzi, 1991) into cooperative care of young), this implies that co- the quasisocial or semisocial categories, because operative breeders can be regarded as "euso- they assume that workers are totipotent. Discovery cial"—just as eusocial insects can be termed "co- of even one behavioral or physiological disconti- operative breeders." nuity, however, would cause such species to sud-

Forum 105 denly shift into the eusocial category. To accurately Vehrencamp's (1979) index of / classify societies according to Crespi and Yancga's (which is closely associated with our skew index) to definitions requires knowing: (1) the behavioral describe the relative importance of personal re- repertoire of all groups of colony members in all production versus indirect fitness effects in soci- social/environmental contexts, and (2) whether eties of cooperative breeders. We have simply ex- there is "obligate complementarity and mutual de- tended this conceptual approach to its logical con- pendency of the castes." This leaves most species clusion. in limbo, because it is rarely known whether some In sum, we agree witii Crespi and Yanega (1995) or all colony members are totipotent in all envi- that it is time to clarify the definition of eusociality. ronments. Further, because Crespi and Yanega in- We believe, however, that it is more appropriate clude physiological attributes in their definition of to expand than to contract the concept Our ap- caste, detailed knowledge of interindividual differ- proach emphasizes convergence and the roles of ences in is also necessary to separate common selective principles underlying social evo- eusocial and cooperatively breeding species. Such lution. The simple, continuous classification system data are difficult to obtain and relationships be- that we propose unites societies exhibiting repro- tween physiological differences and behavioral to- ductive division of labor and alloparental helping tipotency are usually unknown. of kin under a single theoretical and terminological The difficulties of using Crespi and Yanega's umbrella, thus fostering potentially revealing cross- complicated definitional scheme are illustrated by taxa comparisons. We believe this integrated ap- attempts to classify the Polities fuscaius. proach is essential to understanding social evolu- They list it as (facultatively) eusocial, arguing that tion in both vertebrates and invertebrates. workers represent a distinct caste because, unlike foundress queens, workers cannot diapause or Thii article began as a joint project with B. J. Cretpi. We found new . However, Polistts workers do thank him and D. A. Yanega for participating in multiple sometimes found nests (reviewed by Reeve, 1991). exchanges of draft manuscripts, ind for useful commen- Further, there is no evidence that a replacement tary and amicable disagreement. We also thank A. F. G. queen has a smaller behavioral repertoire than a Bourke, G. C Eickwort, J. L. Hoogiand, D. W. Pfennig, foundress, because neither is likely to diapause af- J. S. SheUman-Reeve. N. G. Solomon, K. Tiuji, L. I_ , and several anonymous reviewen for their suggestion*. ter she has been a queen. Thus it is unclear whether Polistes species should be labeled as eusocial or co- We dedicate this paper to the memory of our friend and operatively breeding. mentor George C. Eickwort. His knowledge of natural A second example of these difficulties concerns history and hu ideas, enthusiasm, and good-natured com- mentary were instrumental sources of stimulation and the sweat bee rubicundus. According to encouragement. Yanega (1989), reproductive competence in this species is determined by each female's mating suc- Received 1 August 1993 cess during the first few days after eclosion. Wheth- Revised 2 February 1994 er or not a female mates reportedly depends on Accepted 8 February 1994 the at eclosion. Whereas females that mate become queens, females that do not mate become workers. Crespi and Yanega classify H. rubicundus REFERENCES as (facultatively) eusocial. From an evolutionary Alexander RD, Noonan K, Crespi BJ, 1991. 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