Comparative methods offer powerful insights into social evolution in bees

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<ul><li><p>Comparative methods offer powerful insights into socialevolution in bees</p><p>Sarah D. KOCHER1, Robert J. PAXTON2</p><p>1Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University,Cambridge, MA, USA</p><p>2Institute for Biology, Martin-Luther-University Halle-Wittenberg, Halle, Germany</p><p>Received 9 September 2013 Revised 8 December 2013 Accepted 2 January 2014</p><p>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 fourtimes within the bees. Subsequent elaborations of the reproductive division of labor inherent to eusociality haveled to the evolution of some of the most highly advanced forms of eusociality documented. Likewise, manyreversals 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 commonmechanisms underlying transitions from solitary to group living. In this review, we discuss the extensivebehavioral variation found within the bees and highlight how the comparative method has improved ourunderstanding of social evolution. Finally, we discuss potential difficulties with this approach and outlinepromising avenues for future research.</p><p>comparative method / evolution / communal / semisocial / eusocial / genetics / genomics</p><p>1. INTRODUCTION</p><p>The study of social evolution comprises twocentral questions: the first concerned with theorigins of social behavior and the second withits maintenance in social groups. An under-standing of the factors associated with theorigins and losses of sociality requires acomparative approach that examines evolution-ary transitions in social behavior throughout thephylogeny, while studies of single species cangreatly inform our understanding of some of theprocesses maintaining social traits such as</p><p>reproductive division of labor. In this review,we focus on understanding the first of thesequestions: the evolutionary origins of sociality.We argue that comparative methods can greatlyinform our understanding of both proximatemechanisms and ultimate causes of socialbehavior, and that bees are an ideal group forthese types of studies.</p><p>Though social behavior occurs in a widevariety of contexts when two conspecific ani-mals interact, in the context of social evolutionits use is more often restricted to the coopera-tive, non-agonistic and non-sexual interactionsamong conspecifics sharing a common nest inwhich offspring are reared. Defining sociality inthis way encourages us to address questions ofwhy and how animals form cooperative groups.Though social group formation may bringbenefits to individuals and have many underly-</p><p>Corresponding author: S.D. Kocher,skocher@gmail.comManuscript editor: David Tarpy</p><p>Apidologie Review article* INRA, DIB and Springer-Verlag France, 2014DOI: 10.1007/s13592-014-0268-3</p></li><li><p>ing explanations, social behavior often entailsforfeiting of personal reproduction. It is thisindividual altruism associated with cooperativegroup formation that has been viewed as anevolutionary paradox.</p><p>Eusociality is arguably the most derived formof social behavior with behaviorally discretereproductive castes (i.e., forfeiting of reproduc-tion by workers but not queens), and has heldspecial prominence among evolutionary biologistsbecause it represents one of the major transitionsof life: from a solitary lifestyle to a coordinatedgroup cooperating to reproduce (Maynard Smithand Szathmary 1997). Inclusive fitness remainsthe central theoretical paradigm for understandingsocial evolution and the transition to eusociality(Hamilton 1964; cf. Nowak et al. 2010).</p><p>Though eusociality is taxonomically rare (ca.2 % of insect species are eusocial, Wilson1990), organisms that have achieved this higherlevel of organization frequently meet greatecological success, with eusocial speciesrepresenting approximately 50 % of the worldsinsect biomass (Wilson 1971). Eusociality hasbeen best described in the insect orderHymenoptera, and especially in the bees wheremultiple origins of eusociality have occurredindependently (Figure 1). For this reason, beesare excellent models for studying social evolu-tion within a comparative context.</p><p>Here we present an overview of socialdiversity in bees, explore how a comparativeapproach has aided our understanding of thewhy and how of social evolution, and thendiscuss current problems in this approach andpromising directions for future research.</p><p>1.1. Diversity of social behavior in bees</p><p>Social behavior is commonly categorizedinto six major social types: solitary (lackingsocial behavior), subsocial (those with extendedparental care), communal, semisocial, quasisocial(the latter three collectively called parasocial), andeusocial (Table I). The term eusocial was firstproposed by Susan Batra to describe the socialbehavior of some halictine bees (Batra 1966b).Wilson (1971) expanded the definition of eusoci-</p><p>ality to describe all societies with three maincharacteristics: overlapping generations, coopera-tive brood care, and a reproductive division oflabor with effectively sterile worker castes.Michener (1974) further subdivided eusocialityinto primitive and advanced. These terms weredesigned to emphasize the differences amongtypes of eusocial societies: those with highdegrees of morphological differentiation betweenqueens and workers (advanced, e.g., Apismellifera), and those with less clearly differenti-ated castes based primarily on size (primitive,e.g., paper wasps or halictid bees). The manyforms of social behavior that have evolved withinbees arguably reflect greater social lability than inany other group in the Hymenoptera (Table II).</p><p>Many species of solitary bee nest in aggre-gations where each female constructs her ownnest in close proximity to other females nests.This leads to the grouping of nests into anaggregation, and is often characteristic of manyground nesting bees, including members ofmost of the major bee families/subfamilies:Andrenidae, Apidae (including the Anthophorinaeand the Apinae), Colletidae, Halictidae, andMellitidae (Knerer and Plateaux-Quenu 1966;Wilson 1971; Michener 1974; Stark 1992;Plateaux-Quenu 1993a; Rehan et al. 2010). Oneexplanation for aggregated nesting may be limiteddistribution of suitable substrate in which toconstruct a nest; another is hypothesized to bedefense against parasites through the selfish herd,though the data are equivocal on this point (Batra1966b; Michener 1969; Wilson 1971; Rosenheim1990). While not strictly social, aggregated nestingrequires tolerance of neighbors as well asrecognition of own versus conspecific nests,traits that may be precursors to the highlycooperative behavior and refined nestmate dis-crimination abilities described in eusocial bees(Michener 1974; Spessa et al. 2000; Nowak etal. 2010; Cardinal and Danforth 2011).</p><p>Parasocial colonies, consisting of adultsgenerally from a single generation, have beendescribed extensively in the bees. One exampleof a parasocial lifestyle, communal nesting,occurs when a number of females provisionand lay their own eggs (e.g., without castes) in a</p><p>S.D. Kocher and R.J. Paxton</p></li><li><p>shared nest. Communality is taxonomicallywidespread, and has been documented in theMellitidae, Halictidae, Andrenidae, Apidae,Colletidae, and Megachilidae. Other types ofparasocial behavior have also been character-ized, such as associations between multiplefemales during the breeding season with somedegree of reproductive division of labor (Knererand Plateaux-Quenu 1966; Batra 1966a; Stark1992; Plateaux-Quenu 1993a; Ulrich et al.2009; Rehan et al. 2010). Parasocial associa-tions have been documented in several tribeswithin Apidae (Xylocopini, Allodapini, Ceratinini,and Euglossini), Halictidae (Halictinae), andColletidae (Hyalinae) (Spessa et al. 2000;Cardinal and Danforth 2011; Danforth et al.2013). Often these interactions involve cooperativefounding of nests by two or more females (e.g.,Halictus scabiosae, Batra 1966a; Wilson andHolldobler 2005; Ulrich et al. 2009), or a divisionof labor where some females guard the nest while</p><p>others forage and lay eggs (e.g., Xylocopini/Xylocopa sulcatipes, Stark 1992; Schwarz et al.2011; Ceratinini/Ceratina spp., Rehan et al. 2009).</p><p>Only a small proportion of bee species (ca.6 %, Danforth 2007) are eusocial with a cleardivision of labor established and maintained byone or a few reproductive individuals (Figure 1;Table II). Unlike the parasocial colonies de-scribed above, eusocial nests consist of distin-guishable reproductive castes that cooperate inbrood care. These castes are composed of adultindividuals from two overlapping generationsthat are both potentially able to reproduce(typically mothers and daughters).</p><p>Some lineages, such as the honey bees andstingless bees, represent highly derived forms ofeusociality where large colony sizes, morpho-logical caste dimorphism, and a developmental-ly determined reproductive division of labor arewell established. Based on the current phylog-eny, no reversals to a solitary life history can be</p><p>mya 235 201 176 161 145 100 65 55 34 23 5Triassic Jurassic Cretaceous Paleogene Neogene</p><p>Late Late LateEarlyMiddleEarly Paleocene Eocene Oligocene Miocene</p><p>Isoptera</p><p>Vespinae</p><p>Formicidae</p><p>Allodapini</p><p>Vespid wasps</p><p>Bees</p><p>Termites</p><p>Ants</p><p>Halictini</p><p>Augochlorini</p><p>Halictidae</p><p>Apidae</p><p>Xylocopini</p><p>Ceratinini</p><p>Manuellini</p><p>Bombini</p><p>Meliponini</p><p>Apini</p><p>Euglossini</p><p>Primitive eusocial</p><p>Advanced eusocial</p><p>Solitary</p><p>Solitary and primitive eusocial</p><p>Primitive and advanced eusocial</p><p>Lasioglossum</p><p>Halictus</p><p>Stenogastrinae</p><p>Crabronidae</p><p>Corbiculates</p><p>Xylocopinae</p><p>*</p><p>*</p><p>*</p><p>*</p><p>Spheciform wasps</p><p>Polistinae*</p><p>*</p><p>*</p><p>*</p><p>*</p><p>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 thetemporal range at which each gain or loss has been estimated. Dates and references are documented inTable II.</p><p>Comparative approaches to sociality</p></li><li><p>inferred among these extant, highly eusociallineages (Schwarz et al. 2007). This suggeststhat these species may have crossed an evolu-tionary point of no return (Wilson andHolldobler 2005) which may entail the loss ofreproductive capabilities in workers.</p><p>Other bee lineages, such as halictids andxylocopines, have seemingly less-derived formsof eusocial behavior with smaller colony sizes.Colonies are often annual and founded solitarily bythe queen: they become eusocial as their ontoge-netic end-point. These species lack (or have lowerlevels of) morphological caste dimorphism, andworkers have the ability to mate and lay fertilized,</p><p>female-destined eggs. In halictids and xylocopines,reversions from eusociality back to solitary lifehistories are widespread. This often results in agreat deal of variation in social structure within andbetween species (Figure 1; e.g., Halictinae andXylocopinae, Wcislo and Danforth 1997; Schwarzet al. 2007). Allodapines, in contrast, seem not toexhibit reversions to a solitary lifestyle (Chenowethet al. 2007).</p><p>Based on our current understanding of thephylogenetic relationships within the bees,eusociality appears to have arisen four timesindependently (twice in Apidae and twice inHalictidae) with many subsequent modifications</p><p>Table I. Definitions of social behavior in the literature.</p><p>Alloparentalcare</p><p>Reproductivedivision oflabor</p><p>Overlappingadultgenerations</p><p>Further descriptors References</p><p>Solitary May nest inaggregations</p><p>Michener 1969</p><p>Subsocial Extended parentalcare</p><p>Michener 1969</p><p>Parasocial Communal Females sharenesting area</p><p>Michener 1969</p><p>Quasisocial + Michener 1969Semisocial + + Michener 1969</p><p>Social + Any group livingspecies withreciprocalcommunication of acooperative nature</p><p>Costa &amp;Fitzgerald 1996;Wilson 1971</p><p>Eusocial Primitivelyeusocial</p><p>+ + + Reproductive and non-reproductive castesare morphologicallyindistinguishable</p><p>Michener 1969</p><p>Workers typicallycapable of mating</p><p>Wilson 1971</p><p>Advancedor highlyeusocial</p><p>+ + + High degree ofmorphologicalvariation betweencastes</p><p>Michener 1969</p><p>Workers typicallyincapable of mating</p><p>Wilson 1971</p><p>Facultativelyeusocial</p><p>+ + + The reproductivecaste is totipotentand/or capable ofsurviving on its own</p><p>Crespi &amp; Yanega1995</p><p>Obligatelyeusocial</p><p>+ + + Both castes aremutually dependenton each other</p><p>Crespi &amp; Yanega1995</p><p>Modified from Michener (1974)</p><p>S.D. Kocher and R.J. Paxton</p></li><li><p>TableII.The</p><p>evolutionof</p><p>major</p><p>eusocialclades.</p><p>Group</p><p>Clade</p><p>Socialtransition</p><p>N(Eusocial)</p><p>Est.date</p><p>Range</p><p>Geologicalperiod</p><p>Reference</p><p>Bees</p><p>Corbiculates*</p><p>Solitary</p><p>Primitive</p><p>711</p><p>8778</p><p>95</p><p>LateCretaceous</p><p>Cardinal&amp;</p><p>Danforth2011</p><p>Apini</p><p>Primitive</p><p>Advan</p><p>ced</p><p>1122</p><p>163</p><p>0OligoceneMiocene</p><p>Cardinal&amp;</p><p>Danforth2011;L</p><p>oetal.</p><p>2010</p><p>Meliponini</p><p>Primitive</p><p>Advan</p><p>ced</p><p>500</p><p>5856</p><p>61</p><p>Early</p><p>Eocene</p><p>Cardinal&amp;</p><p>Danforth2011</p><p>Bom</p><p>bini</p><p>Primitive</p><p>Primitive</p><p>a200</p><p>2112</p><p>31</p><p>OligoceneMiocene</p><p>Cardinal&amp;</p><p>Danforth2011</p><p>Euglossini</p><p>Primitive</p><p>Solitary</p><p>028</p><p>2135</p><p>OligoceneMiocene</p><p>Cardinal&amp;</p><p>Danforth2011</p><p>Xylocopinae*</p><p>Solitary</p><p>Primitive</p><p>253+</p><p>9989</p><p>111</p><p>LateCretaceous</p><p>Rehan</p><p>etal.2012</p><p>Allodapini</p><p>Primitive</p><p>advan</p><p>ced</p><p>b250+</p><p>5345</p><p>59</p><p>PaleoceneE</p><p>ocene</p><p>Rehan</p><p>etal.2012</p><p>Ceratinini</p><p>Primitive</p><p>Solitary</p><p>34?</p><p>5143</p><p>57</p><p>PaleoceneE</p><p>ocene</p><p>Rehan</p><p>etal.2012</p><p>Manuellini</p><p>Primitive</p><p>Solitary</p><p>046</p><p>3954</p><p>PaleoceneE</p><p>ocene</p><p>Rehan</p><p>etal.2012</p><p>Xylocopini</p><p>Primitive</p><p>Solitary</p><p>050</p><p>4262</p><p>PaleoceneE</p><p>ocene</p><p>Rehan</p><p>etal.2012</p><p>Halictini*</p><p>Solitary</p><p>Primitive</p><p>300+</p><p>3538</p><p>43</p><p>OligoceneMiocene</p><p>Brady</p><p>etal.2006;Gibbs</p><p>etal.2012</p><p>Augochlorini*</p><p>Solitary</p><p>Primitive</p><p>25+</p><p>2012</p><p>29</p><p>OligoceneMiocene</p><p>Brady</p><p>etal.2006</p><p>Apoid</p><p>Wasps</p><p>Crabronidae</p><p>Solitary</p><p>Primitive</p><p>50</p><p>WenzelandPickering</p><p>1991;Ross</p><p>&amp;Matthew</p><p>s1991</p><p>Vespoid</p><p>Wasps</p><p>Polistinae</p><p>+Vespinae</p><p>Solitary</p><p>Advan</p><p>ced</p><p>880</p><p>&gt;65</p><p>WenzelandPickering</p><p>1991;Hines</p><p>etal.2007</p><p>Stenogastrinae</p><p>Solitary</p><p>Primitive</p><p>&gt;65</p><p>WenzelandPickering</p><p>1991;Hines</p><p>etal.2007</p><p>Ants</p><p>Formicidae</p><p>Solitary</p><p>Advan</p><p>ced</p><p>11,000</p><p>120</p><p>115135</p><p>Early</p><p>Cretaceous</p><p>Brady</p><p>etal.2006;Johnsonetal.2013</p><p>Termites</p><p>Isoptera</p><p>Solitary</p><p>Advan</p><p>ced</p><p>2,200</p><p>200</p><p>180230</p><p>LateTriassicEarly</p><p>Jurassic</p><p>Ware2010</p><p>Thrips</p><p>Thysanoptera</p><p>Solitary</p><p>Primitive</p><p>66.32</p><p>5.25</p><p>9.36</p><p>MioceneP</p><p>liocene</p><p>McLeish</p><p>&amp;Chapm</p><p>an2007</p><p>Aphids</p><p>Hom</p><p>opterac</p><p>Solitary</p><p>Primitive</p><p>60</p><p>Pike&amp;</p><p>Foster2008</p><p>Ambrosiabeetles</p><p>Platypodinae</p><p>Solitary</p><p>Primitive</p><p>2</p><p>Kent&amp;</p><p>Simpson</p><p>1992;B</p><p>iederm</p><p>ann</p><p>&amp;Taborsky</p><p>2011</p><p>Asterisks</p><p>indicatedindependentoriginsof</p><p>eusociality</p><p>within</p><p>thebees.Notethatthesocialtransition</p><p>columnrepresentsthemostextrem</p><p>eform</p><p>sof</p><p>sociality</p><p>foundwithin</p><p>thegroup</p><p>aAlthough</p><p>definitions</p><p>donotallowus</p><p>toexpand</p><p>onwhatw</p><p>eseeasatransitiontoamoresophisticated</p><p>form</p><p>ofeusociality</p><p>inBom</p><p>bus,socialbehaviorinthisgroupincludesanumberoftraits</p><p>oftenassociated</p><p>with</p><p>advanced</p><p>eusociality,including</p><p>theproductionof</p><p>queenpherom</p><p>ones,occasionalswarmfounding,therm</p><p>oregulation,andcoordinatedforaging</p><p>byworkers</p><p>bSom</p><p>emorphologicalspecializationam</p><p>ongcastes</p><p>appearsto</p><p>have</p><p>occurred</p><p>atleastonce</p><p>(and</p><p>perhapstwice)</p><p>inallodapine</p><p>species...</p></li></ul>