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Mechanisms of social evolution: linking adaptative
function with proximate mechanisms
David Tarpy, Stanley Schneider
To cite this version:
Mechanisms of social evolution: linking adaptative
function with proximate mechanisms
David R. TARPY1,Stanley S. SCHNEIDER2
1
Department of Entomology, North Carolina State University, Campus Box 7613, Raleigh, NC 27695-7613, USA
2
Department of Biological Sciences, University of North Carolina, Charlotte, NC 28262, USA
1. INTRODUCTION
Just over 50 years ago, Niko Tinbergen (1963) published his landmark paper in which he posed “four questions” for studying etholo-gy. These questions individually address causa-tion, ontogeny, adaptacausa-tion, and phylogeny, and collectively provide complementary insights contributing to a comprehensive, multifaceted understanding of a particular behavioral charac-teristic (Bateson and Laland 2013). These questions—with their emphasis on an empirical approach to understanding proximate (ontoge-ny; causation) and ultimate (adaptation; phylog-eny) explanations—form the cornerstone of animal behavior as a discipline and have been particularly relevant to the study of the social behavior of bees. Levels of social organization are highly variable among bee species, ranging from solitary to highly eusocial, which makes bees excellent model organisms for both prox-imate and ultprox-imate approaches to understanding social organization and evolution.
Earlier works on bee sociality tended to focus on phylogeny and, especially, adaptation, with a particular emphasis on the role of haplodiploidy and kin selection in the evolution of worker
reproductive altruism (Crozier and Pamilo,
1996). This emphasis on ultimate factors result-ed in an enormous body of theoretical and empirical work that remains a model for the study of social evolution in all animal taxa. However, our knowledge of the proximate mechanisms of bee sociality lagged by compar-ison, largely because of a lack of methodologies for investigating the genetic and molecular bases of social behavior. This changed with the “molecular biology revolution” and the sequencing of the genomes of the honeybee, Apis mellifera (Weinstock et al., 2006) and other species, which ushered in an era of unprecedented opportunities for exploring not only the genetic basis for the organization of a particular social system but also the individual genes and gene complexes of solitary and primitively social species that have been co-opted in the evolution of the advanced insect societies.
Our growing understanding of the molecular basis of social behavior allows for an increas-ingly sophisticated integration of Tinbergen’s four questions (Figure1), and it is in this spirit that we present this special issue. Our goals are to provide reviews and novel empirical studies that integrate molecular and evolutionary ap-proaches to studying bee social behavior, identify common themes in bee social evolu-tion, and propose future areas of research. In Corresponding author: D. Tarpy,
david_tarpy@ncsu.edu
keeping with the historical development of our understanding of social evolution, we have organized this issue to begin with examinations of ultimate causation in bee social evolution and move toward increasingly proximate molecular and genetic mechanisms of sociogenomics.
2. ADVANCES IN SOCIAL MECHANISMS
One of the most insightful approaches to deep evolutionary questions is through the comparative method, and this is no different for studying social evolution. Indeed, the fact that eusociality has evolved independently at least 12 times in multiple taxa (Wilson and Holldobler,2005) provides a wealth of compar-ative data for identifying common threads in social evolution. Whereas ants and termites are ubiquitously eusocial, the bees are particularly well suited as a study group because they span the entire spectrum of social organization from solitary to some of the most advanced societies in animals. Using the comparative approach, Kocher and Paxton (2014) provide a framework for understanding the transition from solitary to social forms in bees by mapping social traits onto phylogenies. Additionally, they also show how modern tools have facilitated the compar-ative approach in ecological and genomic studies, whereby specific genes can be com-pared across different social forms in different contexts. Such comparisons provide deep in-sights into the evolutionary history of social behavior one mechanism at a time.
The comparative approach may address broad patterns in evolution, but the adaptationist paradigm focuses on individual and social reproduction. The next series of articles in this special issue use molecular and sociogenomic approaches to investigate the proximate and ultimate factors shaping the evolution of repro-ductive strategies in the social bees. For example, Goudie and Oldroyd (2014) explore thelytoky (the parthenogenetic production of females). Although rare in honeybees, thelytoky is ubiquitous in the subspecies, Apis mellifera capensis (the Cape honeybee), and is controlled
by perhaps a single genetic locus associated with the differential splicing of a transcription factor. Thelytoky gives workers the potential for producing fertile female offspring and provides opportunities for alternate reproductive strate-gies, including a unique form of social parasit-ism in which a highly invasive, parasitic clone acts as a “transmissible cancer” that inevitably causes the death of the host colony. However, thelytoky presents challenges for maintaining heterozygosity and also generates worker– queen conflict that undermines the cooperation necessary for colony success. Consequently, thelytoky in the Cape bee provides numerous avenues for exploring the evolution of repro-ductive strategies in honeybees, as well as the different levels of selection that have shaped honeybee social organization. Similarly, Grozinger et al. (2014) explore the proximate and ultimate factors governing one of the most spectacular examples of collective activity in the animal kingdom: the simultaneous coordi-nation of thousands of individual honeybee workers and their queen to produce a reproduc-tive swarm and relocate to a new nest site. Inherent to this process is a complex network of chemical and tactile signals, and Grozinger et al. (2014) provide a thorough review of the physiological and genomic mechanisms under-pinning the communication signals used to organize swarming and colony movement. Additionally, the authors speculate on the possible evolutionary origins of swarming from preexisting behavioral and physiological pro-grams in honeybees and other insects. They raise the thought-provoking possibility that genomic mechanisms shaped by life-history components of migration, overwintering, esti-vation, and diapause provided the framework for the evolution of one of the most sophisti-cated systems of collective decision making in the living world.
If form follows function, then reproduction is the culmination of basic social function, and few social activities have been more widely studied than foraging behavior. Mattila and Seeley (2014) present an empirical study of the influence of polyandry by honeybee queens
on inspection behavior (the tendency of foragers to revisit a previously utilized food source to see if it is profitable again). They report that, compared to colonies containing only a single patriline, those with multiple patrilines had more inspectors, higher rates of inspection, and greater foraging and recruitment activity for restocked feeders, which resulted in a fourfold increase in foraging effort at the feeder sites. Extreme polyandry by honeybee queens there-fore increases colony ergonomic success by enhancing the ability to track and respond to a dynamic foraging environment, ultimately in-creasing colony survival and reproductive ca-pacity. This study adds to, and provides a comprehensive review of, the growing body of literature that demonstrates the central role of the honeybee mating system in influencing the division of labor and task portioning among workers, and provides further insights into the levels of selection shaping honey bee social evolution.
The remaining articles within the special issue focus on the molecular and genetic mechanisms underlying specific worker and colony-level traits, and explore how these mechanisms may have been co-opted from solitary and primitively social ancestors during social evolution. Rueppell (2014) reviews be-havior syndromes and pleiotropy in social insects, specifically the pollen-hoarding syn-drome and the multidimensional insights that it has provided at the genetic, developmental, physiological, behavioral, and social levels. In doing so, he bridges suborganismal mechanisms with a complex, highly plastic social phenotype,
and provides insights into the evolution of sociality through the reproductive ground-plan hypothesis (e.g., Amdam et al. 2004). Moreover, Dolezal and Toth (2014) review “sociogenomics” of honeybees and other social insects, including the genomics of honeybee division of labor, communication, caste devel-opment, evolution, and colony health, and skillfully integrate this information to generate a detailed understanding of the evolution and proximate mechanisms of honeybee social life. By focusing on “comparative sociogenomics”, Dolezal and Toth (2014) identify common emerging themes in insect social evolution, including (1) the involvement of metabolic pathways (i.e., the insulin/insulin-like signaling) in the evolution of caste and division of labor; (2) the influence of “genetic toolkits” in the evolution of convergent social behaviors; (3) the central role of transcription networks and epigenetics in a wide array of pathway changes that influence behavioral maturation, reproduc-tive strategies, and an age-influenced division of labor; (4) the involvement of large-scale chang-es in brain-gene exprchang-ession patterns in deter-mining behavioral and developmental plasticity and communication behavior; and (5) the importance of olfactory proteins and glandular structures as targets for selection in social insect evolution.
3. FUTURE DIRECTIONS
pace, our ability to investigate the mechanisms of social behavior will be greatly facilitated. Although our current understanding of the molecular and physiological mechanisms of social behavior is in its infancy, continuing work on behavioral differences and phenotypic plasticity within and among different bee species is well positioned to generate novel insights into the evolution of insect societies (Bloch and Grozinger, 2011). In doing so, we will witness the increasing integration of meta-bolic pathways and the reproductive ground plan to explain the evolution of caste, the role of DNA methylation in regulating caste, and division of labor, potential trade-offs between physiological- and social immunity, and the role of genetic tool kits in the evolution of division of labor and decentralized decision making. Our growing understanding of molecular mecha-nisms will undoubtedly blur the boundaries that previously defined Timbergen’s four questions, ultimately producing an integrated, comprehen-sive understanding of how and why eusociality has arisen among bees and other social groups.
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