The evolution and genetics of superorganisms

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Evolution was punctuated by several major events that fundamentally increased the complexity and biodiversity of life. These evolutionary game-changers include the evolution of sex, multicellularity, and sociality. Sociality evolved multiple times in animals and involves division of labour between individuals that cooperate to benefit a group. In solitary species, genetic mutations can influence an individual's traits and these mutations can spread or decline as a function of the individual's fitness. Social animals, however, have collective `superorganismal' traits that are emergent properties of a complex system composed of thousands of genetically distinct individuals interacting together. The evolution and genetics of superorganismal traits are not well understood, in part because the typical tools for studying genetics in solitary organisms are not directly applicable to social animals. Armed with unique population and functional genomic datasets on the honey bee - a model organism for the study of social behaviour and its evolution - I will advance knowledge in sociogenomics by: 1) Evolution and genetics of superorganismal traits: We will integrate functional and quantitative genomic studies with population genomic surveys of positive and negative selection to test explicit hypotheses about the evolution of superorganismal traits in the honey bee. 2) Genetics and consequences of extreme polyandry: Extreme polyandry (multiple mating) is common in many social insects, but the genetics and fitness consequence of this heritable trait is not well understood. We will use genome wide association mapping to identify the genes underlying polyandry in honey bees. We will also directly test the hypothesis that within colony genetic diversity enhances division of labour and colony fitness. 3) The evolution of extreme recombination: A previous study suggested that rates of recombination in social insects tend to be much higher than in solitary insects. We will advance knowledge in this area by carrying out phylogenetically independent comparisons of recombination rates in several groups of social insects and their solitary ancestors, and ask if worker-biased genes tend to reside in recombination hotspots as we previously discovered in honey bees. Finally, we will theoretically evaluate different models for the evolution of hyper recombination rates in social insects. Impact: Our research will provide the first integrative effort to study the genetics and evolution of superorganisms and will also advance knowledge on two common but poorly understood features of eusocial insects: extreme polyandry and recombination. This will lay the foundation for understanding the ultimate and proximate causes of a major transition in biology. Finally, the research will create fertile grounds for a diverse group of trainees to make major research contributions while mastering cutting edge techniques in evolutionary genomics.