Chemoreceptor Evolution in Hymenoptera and Its Implications for the Evolution of Eusociality

GBE Chemoreceptor Evolution in Hymenoptera and Its Implications for the Evolution of Eusociality Xiaofan Zhou1, Antonis Rokas1, Shelley L. Berger2,3,4, Jürgen Liebig5, Anandasankar Ray6, and Laurence J. Zwiebel1,* 1 Department of Biological Sciences, Vanderbilt University 2 Department of Cell and Developmental Biology, University of Pennsylvania 3 Department of Genetics, University of Pennsylvania 4 Department of Biology, University of Pennsylvania 5 School of Life Sciences, Arizona State University, Tempe 6 Department of Entomology, University of California, Riverside *Corresponding author: E-mail: . Abstract Eusocial insects, mostly Hymenoptera, have evolved unique colonial lifestyles that rely on the perception of social context mainly through pheromones, and chemoreceptors are hypothesized to have played important adaptive roles in the evolution of sociality. However, because chemoreceptor repertoires have been characterized in few social insects and their solitary relatives, a comprehensive examination of this hypothesis has not been possible. Here, we annotate ~3,000 odorant and gustatory receptors in recently sequenced Hymenoptera genomes and systematically compare >4,000 chemoreceptors from 13 hymenopterans, representing one solitary lineage (wasps) and three independently evolved eusocial lineages (ants and two bees). We observe a strong general tendency for chemoreceptors to expand in Hymenoptera, whereas the specifics of gene gains/losses are highly diverse between lineages. We also find more frequent positive selection on chemoreceptors in a facultative eusocial bee and in the common ancestor of ants compared with solitary wasps. Our results suggest that the frequent expansions of chemoreceptors have facilitated the transition to eusociality. Divergent expression patterns of odorant receptors between honeybee and ants further indicate differential roles of chemoreceptors in parallel trajectories of social evolution. Key words: chemosensation, odorant receptor, gustatory receptor, eusociality, Hymenoptera. Introduction Chemosensation, or the perception of chemical cues (e.g. smell and taste) from biotic and abiotic sources, is fundamental to many aspects of insect lifecycles such as host-seeking (e.g. for blood-feeding mosquitoes), mating choice, and searching for oviposition sites (Suh et al. 2014). In social insects, where multiple individuals live as a group and cooperate on tasks like brood care and colony defense, chemosensation serves a particularly important role in mediating the recognition and communication between members of the same society (Wilson 1965). For instance, ants and other eusocial insects form sophisticated societies organized according to specialized behavioral castes, notably the reproductive caste (queen) and sterile caste (worker). The intricate interactions within and between castes that maintain the organization of such societies are coordinated via various types of signals such as chemical (e.g. queen pheromones) as well as acoustical and visual (e.g. the dance language in honeybee) cues (Seeley 1995; Slessor et al. 2005). Chemical communication is perhaps the most universal and important one of such mechanisms, and largely involves the accurate discrimination of a diverse set of cuticular hydrocarbons (CHCs) (Blomquist and Bagneres 2010). Therefore, it is reasonable to hypothesize that the sophisticated chemosensory systems in social insects, and their underlying molecular components, represent adaptations that have facilitated the evolution of sociality (LeBoeuf et al. 2013). A key step in insect chemosensation is the detection of chemicals by receptor proteins present on peripheral sensory ß The Author(s) 2015. 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 License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Genome Biol. Evol. 7(8):2407–2416. doi:10.1093/gbe/evv149 Advance Access publication August 12, 2015 2407 Accepted: July 25, 2015 GBE Zhou et al. demolitor (Burke et al. 2014); one socially polymorphic halictid bee, Lasioglossum albipes (Kocher et al. 2013), which represents another independent origin of eusociality in addition to honeybee and ants; and several additional ant species, notably the dorylomorph Cerapachys biroi which represents the second most early-branching ant species following the ponerine Harpegnathos saltator (Oxley et al. 2014; Schrader et al. 2014; Mikheyev and Linksvayer 2015). These new genomes provide powerful comparative genomics resources to study the evolutionary patterns of chemoreceptor genes in solitary and social insects. Here, we report characterization of the Or and Gr repertoires in eight hymenopteran genomes where careful chemoreceptor annotations were previously lacking. We focused on Or and Gr gene families because they showed more dramatic copy number variations among previously analyzed hymenopteran genomes (Zhou et al. 2012). By comparing >4,000 Ors and Grs from 13 solitary and social Hymenoptera species, we further investigated the evolution of hymenopteran chemoreceptor genes at levels of copy number dynamics, sequence evolution, and expression divergence. Materials and Methods Gene Annotation Genome assemblies of the eight hymenopteran species listed in table 1 were downloaded from their respective sources (supplementary table S8, Supplementary Material online). Or and Gr genes were annotated in these species as described previously (Zhou et al. 2012). In brief, protein sequences of previously reported insect Or and Gr genes were used as queries to perform TBLASTN (Nicholas et al. 1997) search (e value cutoff of 1e-5) against each of the eight hymenopteran genome. Putative Or and Gr coding regions were identified from the search results after filtering out low-scoring and short hits. For each putative coding region, the most similar query sequence was used as reference for homologybased gene prediction using GeneWise v2.2.0 (Birney et al. 2004). All predicted gene models were checked for the presence of the characteristic domains of Ors (IPR004117) or Grs (IPR009318 or IPR013604) in their coded protein sequences using InterProScan v5 (Jones et al. 2014). Previously annotated chemoreceptor genes of N. vitripennis (Robertson et al. 2010), A. mellifera (Robertson and Wanner 2006), and five other ants (Smith, Zimin, et al. 2011; Smith, Smith, et al. 2011; Zhou et al. 2012; Oxley et al. 2014) were used for this study. Genes encoding proteins no shorter than 350 amino acids were included in subsequent phylogenetic and selection analyses. It should be noted that C. obscurior and M. pharaonis have their genomes sequenced most recently during the preparation of this manuscript. The chemore (...truncated)