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

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.

Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication

“…Our findings, taken together with those of previous evolutionary studies (31,39), suggest that dynamic gene family evolution, including gene expansion and sequence evolution, has played an essential role in the evolution of ant communication and sociality. This discovery provides further evidence for the importance of chemical communication in ant biology, as well as a striking example of the role of novel genes in the evolution of social behavior.…”

“…Additionally, Zhou et al (39) found that the 9-exon subfamily has the highest selection coefficient of all ant OR subfamilies. Although some analyses have indicated that ant ORs do not undergo higher positive selection than those of solitary hymenopterans (39, 43), Zhou et al (39) found evidence for higher positive selection in ORs in the ancestors of extant ants, consistent with our finding of rapid gene expansion along that branch.…”

“…The OR gene repertoire has expanded more than threefold in the ancestors of ants (27,31,39). However, evolutionary histories of individual gene lineages have not been systematically investigated.…”

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…In this study, we concentrated particularly on two hallmarks of insect eusociality, as previously described for Hymenoptera, with the expectation that similar patterns occurred along with the emergence of termites. These are the evolution of a sophisticated chemical communication, which is essential for the functioning of a eusocial insect colony 3,14,15 , and major changes in gene regulation along with the evolution of castes 9,10 . We also tested whether transposable elements spurred the evolution of gene families that were essential for the transition to eusociality.…”

Genes and genomic processes underpinning the social lives of ants

“…Some chemical communication genes likely have highly conserved functions as indicated by conserved sequences and antennal expression of core sets of single-ortholog odorant binding proteins (OBPs) and chemosensory proteins (CSPs) [58,59]. However, among the 330 AE 26 (mean AE standard deviation) odorant and the 80 AE 67 gustatory receptors identified in each of eight ant species, >30% were taxonspecific [60]. Frequent gene duplications and losses suggest that many chemical communication genes are involved in adaptive processes in response to changing environments or arms races.…”