Mechanisms of Social Evolution: Linking Adaptative Function with Proximate Mechanisms David Tarpy, Stanley Schneider

Mechanisms of social evolution: linking adaptative function with proximate mechanisms David Tarpy, Stanley Schneider

To cite this version:

David Tarpy, Stanley Schneider. Mechanisms of social evolution: linking adaptative function with proximate mechanisms. Apidologie, Springer Verlag, 2014, 45 (3), pp.285-288. 10.1007/s13592-014- 0282-5. hal-01234764

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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) 45:285–288 Editorial * INRA, DIB and Springer-Verlag France, 2014 DOI: 10.1007/s13592-014-0282-5

Mechanisms of social evolution: linking adaptative function with proximate mechanisms

1 2 David R. TARPY , Stanley S. SCHNEIDER

1Department of Entomology, North Carolina State University, Campus Box 7613, Raleigh, NC 27695-7613, USA 2Department of Biological Sciences, University of North Carolina, Charlotte, NC 28262, USA

1. INTRODUCTION reproductive altruism (Crozier and Pamilo, 1996). This emphasis on ultimate factors result- Just over 50 years ago, Niko Tinbergen ed in an enormous body of theoretical and (1963) published his landmark paper in which empirical work that remains a model for the he posed “four questions” for studying etholo- study of social evolution in all animal taxa. gy. These questions individually address causa- However, our knowledge of the proximate tion, ontogeny, adaptation, and phylogeny, and mechanisms of bee sociality lagged by compar- collectively provide complementary insights ison, largely because of a lack of methodologies contributing to a comprehensive, multifaceted for investigating the genetic and molecular understanding of a particular behavioral charac- bases of social behavior. This changed with teristic (Bateson and Laland 2013). These the “molecular biology revolution” and the questions—with their emphasis on an empirical sequencing of the genomes of the honeybee, approach to understanding proximate (ontoge- Apis mellifera (Weinstock et al., 2006) and ny; causation) and ultimate (adaptation; phylog- other species, which ushered in an era of eny) explanations—form the cornerstone of unprecedented opportunities for exploring not animal behavior as a discipline and have been only the genetic basis for the organization of a particularly relevant to the study of the social particular social system but also the individual behavior of bees. Levels of social organization genes and gene complexes of solitary and are highly variable among bee species, ranging primitively social species that have been co- from solitary to highly eusocial, which makes opted in the evolution of the advanced insect bees excellent model organisms for both prox- societies. imate and ultimate approaches to understanding Our growing understanding of the molecular social organization and evolution. basis of social behavior allows for an increas- Earlier works on bee sociality tended to focus ingly sophisticated integration of Tinbergen’s on phylogeny and, especially, adaptation, with a four questions (Figure 1), and it is in this spirit particular emphasis on the role of haplodiploidy that we present this special issue. Our goals are and kin selection in the evolution of worker to provide reviews and novel empirical studies that integrate molecular and evolutionary approaches to studying bee social behavior, Corresponding author: D. Tarpy, identify common themes in bee social evolu- [email protected] tion, and propose future areas of research. In 286 D.R. Tarpy and S.S. Schneider keeping with the historical development of our by perhaps a single genetic locus associated understanding of social evolution, we have with the differential splicing of a transcription organized this issue to begin with examinations factor. Thelytoky gives workers the potential for of ultimate causation in bee social evolution and producing fertile female offspring and provides move toward increasingly proximate molecular opportunities for alternate reproductive strate- and genetic mechanisms of sociogenomics. gies, including a unique form of social parasit- ism in which a highly invasive, parasitic clone “ ” 2. ADVANCES IN SOCIAL acts as a transmissible cancer that inevitably MECHANISMS causes the death of the host colony. However, thelytoky presents challenges for maintaining – One of the most insightful approaches to heterozygosity and also generates worker deep evolutionary questions is through the queen conflict that undermines the cooperation comparative method, and this is no different necessary for colony success. Consequently, for studying social evolution. Indeed, the fact thelytoky in the Cape bee provides numerous that eusociality has evolved independently at avenues for exploring the evolution of repro- least 12 times in multiple taxa (Wilson and ductive strategies in honeybees, as well as the Holldobler, 2005) provides a wealth of compar- different levels of selection that have shaped ative data for identifying common threads in honeybee social organization. Similarly, social evolution. Whereas ants and termites are Grozinger et al. (2014) explore the proximate ubiquitously eusocial, the bees are particularly and ultimate factors governing one of the most well suited as a study group because they span spectacular examples of collective activity in the entire spectrum of social organization from the animal kingdom: the simultaneous coordi- solitary to some of the most advanced societies nation of thousands of individual honeybee in animals. Using the comparative approach, workers and their queen to produce a reproduc- Kocher and Paxton (2014) provide a framework tive swarm and relocate to a new nest site. for understanding the transition from solitary to Inherent to this process is a complex network of social forms in bees by mapping social traits chemical and tactile signals, and Grozinger et onto phylogenies. Additionally, they also show al. (2014) provide a thorough review of the how modern tools have facilitated the compar- physiological and genomic mechanisms under- ative approach in ecological and genomic pinning the communication signals used to studies, whereby specific genes can be com- organize swarming and colony movement. pared across different social forms in different Additionally, the authors speculate on the contexts. Such comparisons provide deep in- possible evolutionary origins of swarming from sights into the evolutionary history of social preexisting behavioral and physiological pro- behavior one mechanism at a time. grams in honeybees and other insects. They The comparative approach may address raise the thought-provoking possibility that broad patterns in evolution, but the adaptationist genomic mechanisms shaped by life-history paradigm focuses on individual and social components of migration, overwintering, esti- reproduction. The next series of articles in this vation, and diapause provided the framework special issue use molecular and sociogenomic for the evolution of one of the most sophisti- approaches to investigate the proximate and cated systems of collective decision making in ultimate factors shaping the evolution of repro- the living world. ductive strategies in the social bees. For If form follows function, then reproduction is example, Goudie and Oldroyd (2014) explore the culmination of basic social function, and thelytoky (the parthenogenetic production of few social activities have been more widely females). Although rare in honeybees, thelytoky studied than foraging behavior. Mattila and is ubiquitous in the subspecies, Apis mellifera Seeley (2014) present an empirical study of capensis (the Cape honeybee), and is controlled the influence of polyandry by honeybee queens Mechanisms of social evolution 287

Figure 1. Tinbergen’s “four questions” have traditionally provided the theoretical context for studies in the evolution of sociality in bees. Because of modern advances in sociogenomics, researchers have been making more integrative advances seamlessly linking mechanisms across multiple levels of biological organization. on inspection behavior (the tendency of foragers and provides insights into the evolution of to revisit a previously utilized food source to see sociality through the reproductive ground-plan if it is profitable again). They report that, hypothesis (e.g., Amdam et al. 2004). compared to colonies containing only a single Moreover, Dolezal and Toth (2014) review patriline, those with multiple patrilines had “sociogenomics” of honeybees and other social more inspectors, higher rates of inspection, and insects, including the genomics of honeybee greater foraging and recruitment activity for division of labor, communication, caste devel- restocked feeders, which resulted in a fourfold opment, evolution, and colony health, and increase in foraging effort at the feeder sites. skillfully integrate this information to generate Extreme polyandry by honeybee queens there- a detailed understanding of the evolution and fore increases colony ergonomic success by proximate mechanisms of honeybee social life. enhancing the ability to track and respond to a By focusing on “comparative sociogenomics”, dynamic foraging environment, ultimately in- Dolezal and Toth (2014) identify common creasing colony survival and reproductive ca- emerging themes in insect social evolution, pacity. This study adds to, and provides a including (1) the involvement of metabolic comprehensive review of, the growing body of literature that demonstrates the central role of pathways (i.e., the insulin/insulin-like signaling) the honeybee mating system in influencing the in the evolution of caste and division of labor; “ ” division of labor and task portioning among (2) the influence of genetic toolkits in the workers, and provides further insights into the evolution of convergent social behaviors; (3) the levels of selection shaping honey bee social central role of transcription networks and evolution. epigenetics in a wide array of pathway changes The remaining articles within the special that influence behavioral maturation, reproduc- issue focus on the molecular and genetic tive strategies, and an age-influenced division of mechanisms underlying specific worker and labor; (4) the involvement of large-scale chang- colony-level traits, and explore how these es in brain-gene expression patterns in deter- mechanisms may have been co-opted from mining behavioral and developmental plasticity solitary and primitively social ancestors during and communication behavior; and (5) the social evolution. Rueppell (2014) reviews be- importance of olfactory proteins and glandular havior syndromes and pleiotropy in social structures as targets for selection in social insect insects, specifically the pollen-hoarding syn- evolution. drome and the multidimensional insights that it has provided at the genetic, developmental, 3. FUTURE DIRECTIONS physiological, behavioral, and social levels. In doing so, he bridges suborganismal mechanisms As next-generation sequencing and bioinfor- with a complex, highly plastic social phenotype, matics techniques continue to evolve at a rapid 288 D.R. Tarpy and S.S. Schneider pace, our ability to investigate the mechanisms Bloch, G., Grozinger, C.M. (2011) Social molecular pathways and the evolution of bee societies. R. of social behavior will be greatly facilitated. Soc. Philos. Trans. Biol. Sci. 366(1574), 2155– Although our current understanding of the 2170 molecular and physiological mechanisms of Crozier, R.H., Pamilo, P. (1996) Evolution of social social behavior is in its infancy, continuing insect colonies: sex allocation and kin selection. work on behavioral differences and phenotypic Oxford University Press, New York plasticity within and among different bee Dolezal A.G.,Toth A.L. (2014) Honey bee sociogenomics: a genome-scale perspective on bee species is well positioned to generate novel social behavior and health. Apidologie 45(3), insights into the evolution of insect societies doi:10.1007/s13592-013-0251-4 (Bloch and Grozinger, 2011). In doing so, we Goudie F., Oldroyd B.P. (2014) Thelitoky in the honey will witness the increasing integration of meta- bee. Apidologie 45(3), doi:10.1007/s13592-013- 0261-2 bolic pathways and the reproductive ground Grozinger C.M., Richards J., Mattila H. (2014) From plan to explain the evolution of caste, the role of molecules to societies: mechanisms regulating DNA methylation in regulating caste, and swarming behavior in honey bees (Apis spp.) division of labor, potential trade-offs between Apidologie 45(3): doi:10.1007/s13592-013-0253-2 physiological- and social immunity, and the role Kocher S.D., Paxton R.J. (2014) Comparative methods of genetic tool kits in the evolution of division offer powerful insights into social evolution in bees. Apidologie 45(3), doi:10.1007/s13592-014- of labor and decentralized decision making. Our 0268-3 growing understanding of molecular mecha- Mattila H.R., Seeley T.D. (2014) Extreme polyandry nisms will undoubtedly blur the boundaries that improves a honey bee colony’s ability to track previously defined Timbergen’s four questions, dynamic foraging opportunities via greater activity of inspecting bees. Apidologie 45(3), doi:10.1007/ ultimately producing an integrated, comprehen- s13592-013-0252-3 sive understanding of how and why eusociality Rueppell O. (2014) The architecture of the pollen has arisen among bees and other social groups. hoarding syndrome in honey bees: implications for understanding social evolution, behavioral syndromes, and selective breeding. Apidologie 45(3), REFERENCES doi:10.1007/s13592-013-0244-3 Tinbergen, N. (1963) On aims and methods of ethology. – Amdam, G.V., Norberg, K., Fondrk, M.K., Page, R.E. Zeitschr. Tierpshchol. 20, 410 433 (2004) Reproductive ground plan may mediate Weinstock, G.M., Robinson, G.E., et al. (2006) colony-level selection effects on individual foraging Insights into social insects from the genome of behavior in honey bees. Proc. Natl Acad. Sci. USA the honeybee Apis mellifera.Nature443,931– 101(31), 11350–11355 949 Bateson, P., Laland, K.N. (2013) Tinbergen’s four Wilson, E.O., Holldobler, B. 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