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: . Accepted: July 25, 2015 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 GBE Zhou et al. neuron membrane, which initiate downstream signaling ultimately leading to behavioral responses. Three classes of insect chemosensory receptors are currently known. Odorant receptors (Ors) and gustatory receptors (Grs) belong to the same superfamily and both have seven transmembrane domains. However they differ in their general functions: Ors are generally, but not exclusively, expressed in antenna and other chemosensory appendages where they detect various volatile compounds (Suh et al. 2014); in contrast, Grs display diverse expression patterns in gustatory organs and other tissues, and the few Grs with known function include receptors for sweet and bitter tastants, as well as for carbon dioxide (Suh et al. 2014). The third chemoreceptor class is comprised of ionotropic receptors (Irs), which are members of the ancient ionotropic glutamate receptor family (Benton et al. 2009). Their roles in chemosensation were only recently discovered and known ligands include amines and acids (Koh et al. 2014; Suh et al. 2014). The genes encoding these chemoreceptors have experienced highly dynamic evolution in insects; they are among the most rapidly evolving genes in the genome (Neafsey et al. 2015), and their copy numbers can vary considerably among insect lineages (Sánchez-Gracia et al. 2011). Intriguingly, some of the largest chemoreceptor repertoires are found in eusocial insects. Each of the four ant genomes with available chemoreceptor annotations contains more than 300 Ors as well as 17–97 Grs and 23–32 Irs (Smith, Zimin, et al. 2011; Smith, Smith, et al. 2011; Zhou et al. 2012). The honeybee Apis mellifera also has 163 Ors (Robertson and Wanner 2006), which exceeds most solitary insects (Sánchez-Gracia et al. 2011). We recently compared the chemoreceptor repertoires of selected hymenopteran species and demonstrated that they are largely shaped by rapid gain-andloss throughout the evolution of these lineages (Zhou et al. 2012). In particular, the Or family appears to have experienced a dramatic expansion in the common ancestor of ants (Zhou et al. 2012). Although these findings are consistent with the adaptive role of chemoreceptors in the evolution of social insects, contradictory observations have also been made. For example, the solitary parasitoid jewel wasp Nasonia vitripennis contains ~60 more Ors and ~40 more Grs than A. mellifera (Robertson et al. 2010), seemingly challenging the notion that social insects require a greater variety of chemoreceptors than solitary insects. Additionally, a recent molecular evolutionary comparison of Ors found lower levels of positive selection in ants relative to N. vitripennis (Roux et al. 2014). However, N. vitripennis is the only solitary hyme (...truncated)