Comparative methods offer powerful insights into social evolution in bees Sarah Kocher, Robert Paxton To cite this version: Sarah Kocher, Robert Paxton. Comparative methods offer powerful insights into social evolution in bees. Apidologie, Springer Verlag, 2014, 45 (3), pp.289-305. 10.1007/s13592-014-0268-3. hal- 01234748 HAL Id: hal-01234748 https://hal.archives-ouvertes.fr/hal-01234748 Submitted on 27 Nov 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2014) 45:289–305 Review article * INRA, DIB and Springer-Verlag France, 2014 DOI: 10.1007/s13592-014-0268-3 Comparative methods offer powerful insights into social evolution in bees 1 2 Sarah D. KOCHER , Robert J. PAXTON 1Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA 2Institute for Biology, Martin-Luther-University Halle-Wittenberg, Halle, Germany Received 9 September 2013 – Revised 8 December 2013 – Accepted 2 January 2014 Abstract – Bees are excellent models for studying the evolution of sociality. While most species are solitary, many form social groups. The most complex form of social behavior, eusociality, has arisen independently four times within the bees. Subsequent elaborations of the reproductive division of labor inherent to eusociality have led to the evolution of some of the most highly advanced forms of eusociality documented. Likewise, many reversals back to solitary behavior also create substantial variation in sociality within the bees. These replicated, independent origins and losses enable a comparative approach that facilitates the search for common mechanisms underlying transitions from solitary to group living. In this review, we discuss the extensive behavioral variation found within the bees and highlight how the comparative method has improved our understanding of social evolution. Finally, we discuss potential difficulties with this approach and outline promising avenues for future research. comparative method / evolution / communal / semisocial / eusocial / genetics / genomics 1. INTRODUCTION reproductive division of labor. In this review, we focus on understanding the first of these The study of social evolution comprises two questions: the evolutionary origins of sociality. central questions: the first concerned with the We argue that comparative methods can greatly origins of social behavior and the second with inform our understanding of both proximate its maintenance in social groups. An under- mechanisms and ultimate causes of social standing of the factors associated with the behavior, and that bees are an ideal group for origins and losses of sociality requires a these types of studies. comparative approach that examines evolution- Though social behavior occurs in a wide ary transitions in social behavior throughout the variety of contexts when two conspecific ani- phylogeny, while studies of single species can mals interact, in the context of social evolution greatly inform our understanding of some of the its use is more often restricted to the coopera- processes maintaining social traits such as tive, non-agonistic and non-sexual interactions among conspecifics sharing a common nest in which offspring are reared. Defining sociality in this way encourages us to address questions of Corresponding author: S.D. Kocher, why and how animals form cooperative groups. [email protected] Though social group formation may bring Manuscript editor: David Tarpy benefits to individuals and have many underly- 290 S.D. Kocher and R.J. Paxton ing explanations, social behavior often entails ality to describe all societies with three main forfeiting of personal reproduction. It is this characteristics: overlapping generations, coopera- individual altruism associated with cooperative tive brood care, and a reproductive division of group formation that has been viewed as an labor with effectively sterile worker castes. evolutionary paradox. Michener (1974) further subdivided eusociality Eusociality is arguably the most derived form into ‘primitive’ and ‘advanced’. These terms were of social behavior with behaviorally discrete designed to emphasize the differences among reproductive castes (i.e., forfeiting of reproduc- types of eusocial societies: those with high tion by workers but not queens), and has held degrees of morphological differentiation between special prominence among evolutionary biologists queens and workers (‘advanced’, e.g., Apis because it represents one of the major transitions mellifera), and those with less clearly differenti- of life: from a solitary lifestyle to a coordinated ated castes based primarily on size (‘primitive’, group cooperating to reproduce (Maynard Smith e.g., paper wasps or halictid bees). The many and Szathmary 1997). Inclusive fitness remains forms of social behavior that have evolved within the central theoretical paradigm for understanding bees arguably reflect greater social lability than in social evolution and the transition to eusociality any other group in the Hymenoptera (Table II). (Hamilton 1964; cf. Nowak et al. 2010). Many species of solitary bee nest in aggre- Though eusociality is taxonomically rare (ca. gations where each female constructs her own 2 % of insect species are eusocial, Wilson nest in close proximity to other females’ nests. 1990), organisms that have achieved this higher This leads to the grouping of nests into an level of organization frequently meet great aggregation, and is often characteristic of many ecological success, with eusocial species ground nesting bees, including members of representing approximately 50 % of the world’s most of the major bee families/subfamilies: insect biomass (Wilson 1971). Eusociality has Andrenidae, Apidae (including the Anthophorinae been best described in the insect order and the Apinae), Colletidae, Halictidae, and Hymenoptera, and especially in the bees where Mellitidae (Knerer and Plateaux-Quenu 1966; multiple origins of eusociality have occurred Wilson 1971; Michener 1974;Stark1992; independently (Figure 1). For this reason, bees Plateaux-Quenu 1993a; Rehan et al. 2010). One are excellent models for studying social evolu- explanation for aggregated nesting may be limited tion within a comparative context. distribution of suitable substrate in which to Here we present an overview of social construct a nest; another is hypothesized to be diversity in bees, explore how a comparative defense against parasites through the selfish herd, approach has aided our understanding of the though the data are equivocal on this point (Batra why and how of social evolution, and then 1966b;Michener1969; Wilson 1971; Rosenheim discuss current problems in this approach and 1990). While not strictly social, aggregated nesting promising directions for future research. requires tolerance of neighbors as well as recognition of own versus conspecific nests, 1.1. Diversity of social behavior in bees traits that may be precursors to the highly cooperative behavior and refined nestmate dis- Social behavior is commonly categorized crimination abilities described in eusocial bees into six major social types: solitary (lacking (Michener 1974;Spessaetal.2000; Nowak et social behavior), subsocial (those with extended al. 2010; Cardinal and Danforth 2011). parental care), communal, semisocial, quasisocial Parasocial colonies, consisting of adults (the latter three collectively called parasocial), and generally from a single generation, have been eusocial (Table I). The term ‘eusocial’ was first described extensively in the bees. One example proposed by Susan Batra to describe the social of a parasocial lifestyle, communal nesting, behavior of some halictine bees (Batra 1966b). occurs when a number of females provision Wilson (1971) expanded the definition of eusoci- and lay their own eggs (e.g., without castes) in a Comparative approaches to sociality 291 Lasioglossum Solitary Halictini * Halictidae Halictus Solitary and primitive eusocial Augochlorini Primitive eusocial * Primitive and advanced eusocial Bees Xylocopini Advanced eusocial * Manuellini Xylocopinae Ceratinini Allodapini Apidae Bombini * Meliponini Corbiculates Apini Euglossini Spheciform wasps * Crabronidae Ants * Formicidae Vespinae * Polistinae Vespid wasps * Stenogastrinae Termites * Isoptera LateEarly Middle LateEarly Late Paleocene Eocene Oligocene Miocene Triassic Jurassic Cretaceous Paleogene Neogene mya 235 201 176 161 145 100 65 55 34 23 5 Figure 1. The evolution of major eusocial, extant clades in bees, other Hymenoptera and Isoptera (termites). Clades not shown are solitary or parasocial. Asterisks indicate independent origins of primitive eusociality. Colors indicate the forms of sociality that occur within each group and the lengths of the bars indicate the temporal range at which each gain or loss has been estimated. Dates and references are documented in Table II. shared nest. Communality is taxonomically others forage and lay eggs (e.g., Xylocopini/ widespread, and has been documented in the Xylocopa sulcatipes,Stark1992;