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Changing Paradigms in Insect Social Evolution: Insights from Halictine and Allodapine Bees

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Changing Paradigms in Insect Social Evolution: Insights from Halictine and Allodapine Bees ANRV297-EN52-07 ARI 18 July 2006 2:13 V I E E W R S I E N C N A D V A Changing Paradigms in Insect Social Evolution: Insights from Halictine and Allodapine Bees Michael P. Schwarz,1 Miriam H. Richards,2 and Bryan N. Danforth3 1School of Biological Sciences, Flinders University, Adelaide S.A. 5001, Australia; email: Michael.Schwarz@flinders.edu.au 2Department of Biological Sciences, Brock University, St. Catharines, ON L2S 3A1, Canada; email: [email protected] 3Department of Entomology, Cornell University, Ithaca, New York 14853; email: [email protected] Annu. Rev. Entomol. 2007. 52:127–50 Key Words The Annual Review of Entomology is online at sex allocation, caste determination, phylogenetics, kin selection ento.annualreviews.org This article’s doi: Abstract 10.1146/annurev.ento.51.110104.150950 Until the 1980s theories of social insect evolution drew strongly Copyright c 2007 by Annual Reviews. on halictine and allodapine bees. However, that early work suffered All rights reserved from a lack of sound phylogenetic inference and detailed informa- 0066-4170/07/0107-0127$20.00 tion on social behavior in many critical taxa. Recent studies have changed our understanding of these bee groups in profound ways. It has become apparent that forms of social organization, caste de- termination, and sex allocation are more labile and complex than previously thought, although the terminologies for describing them are still inadequate. Furthermore, the unexpected complexity means that many key parameters in kin selection and reproductive skew models remain unquantified, and addressing this lack of informa- tion will be formidable. At the same time, phylogenetic questions have become more tractable, and DNA sequence-based studies have resolved questions that earlier studies could not resolve, radically changing our understanding of the number of origins and losses of sociality in these bees. 127 ANRV297-EN52-07 ARI 18 July 2006 2:13 INTRODUCTION corbiculate apids, which comprise the orchid bees (Euglossini), bumble bees (Bombini), Many social insect taxa display extreme forms stingless bees (Meliponini), and honey bees Eusociality: of altruism, in which the reproductive tra- (Apini); once in an ancestor of the extant al- reproductive skew jectories of individuals are inflexible and de- lodapine bees (75); and three times within the based on termined before adulthood, leading to sharp generational lines, Halictinae (4, 20). While the corbiculates have reproductive skew between queens and work- mostly entailing been the focus of much work on bee social- ers. Understanding reproductive altruism was reproductive ity, only the euglossines contain species that mothers and a major problem for Darwin and has been a fo- are not eusocial (9). This leaves only the hal- worker-like cus for evolutionary biologists ever since. Try- ictines and allodapines as groups that span the daughters ing to understand how eusociality has evolved full range from solitary to eusocial. Halictines Corbiculate apids: has mostly been the precinct of comparative and allodapines have evolved in different ma- bees in the family biology. Many taxa, such as termites, ants, Apidae with a jor clades of bees (Figure 1), and their bi- stingless bees, and honey bees, are composed corbicula, a “basket” ologies are also different. This review pro- entirely of species in which sociality is com- of setae for vides an overview of recent studies of social transporting pollen plex, obligate, and there are no closely related behavior and evolution in these two important solitary or weakly social taxa. For these groups lineages. it may be difficult or impossible to com- pare the consequences of individual strate- gies involving social and nonsocial options. For such groups it is also difficult to re- Halictines construct feasible pathways that lead from solitary to social living, because remnants of The Halictinae is the largest and most di- transitory stages have been obliterated over verse subfamily in the Halictidae, and among evolutionary time, leaving only hypothetical bees in general, it is the most interesting from solitary starting points and known advanced the perspective of social evolution because of end-states. In addition, there are many other the sheer diversity of social systems it con- taxa in which forms of sociality vary greatly tains (46). The subfamily includes more than within and among species, forms of altruism 2400 species of which we estimate around vary from slight to extreme, and individuals 830 are eusocial. Halictidae has a cosmopoli- are not consigned to specific roles for their tan distribution, with representatives on ev- entire lifetime. These latter groups provide ery continent except Antarctica. Seven gen- the insights needed to understand how more era and subgenera are thought to include advanced forms of sociality evolve (41, 46, 96). obligately eusocialt species: Halictus (Halic- Halictine and allodapine bees have been tus), Halictus (Seladonia), Lasioglossum (Evy- prominent for understanding how sociality laeus), Lasioglossum (Dialictus), Augochlora, Au- has evolved from solitary ancestors for several gochlorella, and Augochloropsis. In most cases, even closely related species show widely dif- reasons: Both groups include (a) many social species with facultative adoption of solitary or fering levels of social organization (94). Most eusocial halictine groups are from the North- social roles by individuals, (b) relatively recent transitions between solitary and social living, ern Hemisphere (e.g., Halictus and Lasioglos- ), whereas the eusocial augochlorines (and and (c) substantial variability in the degree of sum sociality within and between extant species. Augochlorini in general) have their great- est diversity in the neotropical regions. Re- cent reports of eusociality in Augochloropsis BACKGROUND AND NATURAL (11) and facultative eusociality in Megalopta (2, HISTORY 85, 93) suggest that eusociality may be more Eusociality is thought to have arisen at least widespread in the Augochlorini than previ- five times in bees: once or maybe twice in the ously imagined. 128 Schwarz · Richards · Danforth ANRV297-EN52-07 ARI 18 July 2006 2:13 Melittidae Fideliinae Megachilidae Megachilinae Xylocopinae Apidae Nomadinae Apinae Andrenidae Rophitinae Halictidae Nomiinae Nomioidinae Halictinae Figure 1 Phylogeny of the major bee groups with the position of Stenotritidae halictines, allodapines (in Xylocopinae), and the corbiculate Apinae indicated. Modified from Colletidae Danforth et al. (23a). Allodapines Australia, and southern Asia, they have re- ceived relatively little taxonomic attention. The allodapines (tribe Allodapini, subfam- Following Reyes (60) we regard previously ily Xylocopinae, family Apidae) form a rela- recognized subgenera as genera, which means tively small group with at least 250 described that the tribe currently contains 12 genera, of species. They likely contain a much larger which 4 ( , and number of actual species, but because they Inquilina, Effractapis, Eucondylops ) are obligate social parasites. The are largely restricted to sub-Saharan Africa, Nasutapis www.annualreviews.org • Changing Paradigms in Insect Social Evolution 129 ANRV297-EN52-07 ARI 18 July 2006 2:13 Malagasy species currently placed in Halter- decade. The many subsequent proposals for apis form a distinct basal clade (80) and will alternative lexicons are summarized by Costa eventually be accorded generic status. & Fitzgerald (13), though there is little con- Subsociality: extended The allodapines differ from nearly all other sensus with most studies now presenting brief parent-offspring bees in that they do not rear their brood within explanations of the terms that they use and contact during cells—instead larvae are reared in a commu- employing modifiers such as obligately, facul- offspring nal undivided tunnel excavated into the pithy tatively, weakly, and so on. development centers of dead stems and branches or else in In both allodapines and halictines, and Semisociality: similar tunnels excavated by other burrow- many other social taxa, the problem of ascrib- reproductive skew ing insects and then reused by allodapines. ing terms of sociality to species is that relation- among same-generation Most species rear their larvae progressively ships within colonies can vary both between adults that are jointly throughout their development, a trait that is colonies and over time. In the following sec- rearing brood, so also different from nearly all other bees, al- tions we outline how these relationships can that some adults though some species mass provision individ- vary and how this creates difficulties for ap- adopt alloparental ual larvae (45) or groups of larvae (80) or they plying social terminologies to species. roles adopt a mix of mass and progressive provi- sioning strategies (45, 75). Early studies suggested that some allodap- Halictines ines in apparently basal clades were solitary or Because the kind of sociality exhibited in only weakly social, leading to the notion that many species varies widely over the course sociality had evolved de novo within extant of colony development, it is important to un- clades (49, 96). Furthermore, some of these derstand how colony composition can change basal groups were complete or partial mass over time. The diversity of halictine colony provisioners, suggesting that evolution of so- cycles is illustrated in Figure 2. The timing ciality was linked to a transition from mass to of brood production and whether females di- progressive
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