Abstract
Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes experienced reduced selection compared with genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also experienced reduced selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory.
Highlights
Kin selection theory provides the dominant framework for understanding the evolution of diverse types of social behavior, from cooperation to conflict, across the tree of life (Hamilton 1964; Bourke 2011)
While kin selection theory has always had an explicit genetic focus (Hamilton 1964), researchers have made little progress in identifying specific genes that have been shaped by kin selection (Thompson et al 2013; Ronai et al 2016), or in identifying genome-wide evolutionary signatures of kin selection (Van Dyken and Wade 2012; Ostrowski et al 2015)
This shortfall is notable in the social insects because the sterile worker caste is the archetypical example of an altruistic phenotype that evolved through kin selection (Hamilton 1964; Queller and Strassmann 1998; Bourke 2011)
Summary
Kin selection theory provides the dominant framework for understanding the evolution of diverse types of social behavior, from cooperation to conflict, across the tree of life (Hamilton 1964; Bourke 2011). Monomorium pharaonis, a derived ant with obligately sterile workers and many queens per colony (i.e., low within-colony relatedness) (Holldobler and Wilson 1990), in which signatures of kin selection compared with direct selection are expected to be pronounced (Linksvayer and Wade 2009; Linksvayer and Wade 2016), we identified caste-associated genes and studied genomic signatures of short- and long-term molecular evolution of these genes.
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