Queens and Workers Contribute Differently to Adaptive Evolution in Bumble Bees and Honey Bees

GBE Queens and Workers Contribute Differently to Adaptive Evolution in Bumble Bees and Honey Bees Brock A. Harpur1,4, Alivia Dey1, Jennifer R. Albert1, Sani Patel1, Heather M. Hines2, Martin Hasselmann3, Laurence Packer1, and Amro Zayed1,* 1 Department of Biology, York University, Toronto, Canada 2 Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 3 Department of Livestock Population Genomics, Institute of Animal Science, University of Hohenheim, Stuttgart, Germany 4 Present address: Department of Molecular Genetics, University of Toronto, Toronto, Canada. *Corresponding author: E-mail: . Accepted: September 8, 2017 Data deposition: This project has been deposited at NCBI SRA under the accession PRNJA347806 Abstract Eusociality represents a major transition in evolution and is typified by cooperative brood care and reproductive division of labor between generations. In bees, this division of labor allows queens and workers to phenotypically specialize. Worker traits associated with helping are thought to be crucial to the fitness of a eusocial lineage, and recent studies of honey bees (genus Apis) have found that adaptively evolving genes often have worker-biased expression patterns. It is unclear however if worker-biased genes are disproportionately acted on by strong positive selection in all eusocial insects. We undertook a comparative population genomics study of bumble bees (Bombus) and honey bees to quantify natural selection on queen- and worker-biased genes across two levels of social complexity. Despite sharing a common eusocial ancestor, genes, and gene groups with the highest levels of positive selection were often unique within each genus, indicating that life history and the environment, but not sociality per se, drives patterns of adaptive molecular evolution. We uncovered differences in the contribution of queen- and worker-biased genes to adaptive evolution in bumble bees versus honey bees. Unlike honey bees, where worker-biased genes are enriched for signs of adaptive evolution, genes experiencing positive selection in bumble bees were predominately expressed by reproductive foundresses during the initial solitary-founding stage of colonies. Our study suggests that solitary founding is a major selective pressure and that the loss of queen totipotency may cause a change in the architecture of selective pressures upon the social insect genome. Key words: sociality, natural selection, kin selection, fitness. Introduction Within a hymenopteran eusocial colony, labor is divided between the queens—responsible for most of the reproduction—and their workers—responsible for all aspects of colony upkeep including brood care, nest defense, and foraging (Wheeler 1910; Wilson 1985; Winston 1987; Hölldobler and Wilson 1990; Sagili et al. 2011; Wray et al. 2011). The separation and subsequent specialization of these roles is the result of Darwinian selection that has acted directly on mutations contributing to queen phenotypes and indirectly on mutations that influence worker traits (Hamilton 1964a, 1964b; Wilson 1985; Sagili et al. 2011; Wray et al. 2011). We do not yet have an understanding of the relative role of queen or worker phenotypes to the fitness of eusocial lineages, a knowledge gap that has hindered our ability to understand the evolutionary processes responsible for caste divergence across different stages of social evolution and the resulting changes in social complexity. Until recently, it was impossible to objectively compare the fitness effects of mutations influencing queen and worker traits. However, advances in population and functional genomics of social insects have allowed researchers to identify genes that are associated with worker and queen traits and quantify adaptive evolution in social lineages (Hasselmann et al. 2015; Kent and Zayed 2015). ß The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact Genome Biol. Evol. 9(9):2395–2402. doi:10.1093/gbe/evx182 Advance Access publication September 11, 2017 2395 GBE Harpur et al. The first population genomic study of a social insect demonstrated genes with worker biased expression being more commonly under positive selection in the eusocial honey bee, Apis mellifera (Harpur et al. 2014). However, the relative levels of adaptive evolution of worker genes in other eusocial species is not well understood and may be substantially different as a result of variation in social lifestyles and life histories among taxa. In the honey bees (Apis spp.), for example, colonies are perennial and contain thousands of individual workers that are morphologically distinct from their single queen (Michener 1974; Rehan and Toth 2015). In contrast, most bumble bees (Bombus spp.) have small, annual colonies, and have a solitary worker-less phase that precedes early colony development (Michener 1974; Winston 1987; Rehan and Toth 2015). During the worker-less phase, foundresses (future queens) are solely responsible for the success of a future colony’s output and perform all or a subset of the behavioral repertoire of workers to provision their first brood (Alford 1969; Crespi and Yanega 1995; Gadagkar 1997; Bourke 2011; Rehan and Toth 2015). In these annual eusocial societies, the success of a colony may be more influenced by traits expressed by foundresses and queens than those expressed by workers (Michener 1974). The corbiculate bees are an ideal group to study the relative contribution of queen-acting and worker-acting mutations to fitness because of their considerable variation in social organization (Rehan and Toth 2015). Moreover, honey bees and bumble bees share a common social ancestor, and consequently, have been subject to the potential genomic impacts of social evolution for the same length of time (Romiguier et al. 2016). We carried out a comparative population genomics study of bumble bees and honey bees to identify and characterize genes with signatures of adaptive evolution in the two lineages, and compared the fitness effects of nonsynonymous mutations influencing queen and worker phenotypes in the bumble bees relative to the perennially eusocial honey bees. (Sadd et al. 2015) using the default parameters of BWA v 7.5 and SAMtools v 1.19 (Li et al. 2009; Li and Durbin 2010). Because sequences were diverse and divergent relative to the reference genome, we remapped each bee’s sequence using STAMPY v 1.0 (Lunter and Goodson 2011) at a substitution rate of 0.02. We subsequently realigned with GATK v 3.1 RealignerTargetCreator followed by IndelRealigner to re (...truncated)