From molecules to societies and back again: the relationship between social evolution and genome evolution

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The rise of sociality represented a major transition in evolution that puzzled biologists for centuries. Social insects exhibit reproductive altruism: workers forgo reproduction to help their mother reproduce. Current theories for how and why sociality evolved assume a simple model of evolution where the evolution of sociality proceeds independently of genome evolution. However, there is a growing body of evidence showing that derived features of social insect genomes reflect changes caused by sociality. Does social behaviour alter patterns of genome evolution in ways that can enhance or, in some cases, limit the spread of social alleles? ******Our group has led pioneering studies that linked features of genome structure with the evolution of worker traits in honey bees. Over the next five years, we plan to uncover the missing links between social evolution and genome evolution by answering the following questions:******1) Does sociality increase genetic loads? Social populations are predicted to have large reductions in effective size, which weakens the strength of natural selection. As a consequence, social genomes are expected to harbour more slightly deleterious mutations that reduce fitness (i.e. higher genetic load). We will compare genetic diversity and the frequency of deleterious mutations in the sequenced genomes of many social and solitary insects to test this hypothesis. ******2) Does sociality increase mutation rates and biases? Queens tend to be long lived and tend to have high rates of meiotic recombination; both features are expected to influence the mutational process - a fundamental evolutionary parameter. We will quantify and contrast mutational biases in social versus solitary insect genomes. We will also directly estimate the mutation rate in honey bee genomes and study if mutation is linked to high recombination and/or high longevity.******3) Does the sex-determination load limit the evolution of sociality? Ants, bees and wasps have a form of sex determination that imposes a substantial genetic load in small populations. This genetic load may limit or reverse the evolution of sociality: we will test this hypothesis using simulation models that explicitly account for sex determination during social evolution. ******4) What is the mechanistic and evolutionary basis of kin-recognition in bees? We will study this precursor trait for social evolution using a novel combination of targeted genome sequencing, chemical analysis of hydrocarbon scent cues, and behavioral assays of honey bee workers. ******My proposed research has a great potential for changing the way biologists think about sociality by illuminating how social behaviour influences patterns of genome evolution that `feedback' and alter the evolutionary trajectory of social populations. The transformational research proposed herein will help us understand both the rise and rarity of sociality in animals.**