Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

Abstract

BackgroundThe complex societies of ants and other social insects rely on sophisticated chemical communication. Two families of small soluble proteins, the odorant binding and chemosensory proteins (OBPs and CSPs), are believed to be important in insect chemosensation. To better understand the role of these proteins in ant olfaction, we examined their evolution and expression across the ants using phylogenetics and sex- and tissue-specific RNA-seq.ResultsWe find that subsets of both OBPs and CSPs are expressed in the antennae, contradicting the previous hypothesis that CSPs have replaced OBPs in ant olfaction. Both protein families have several highly conserved clades with a single ortholog in all eusocial hymenopterans, as well as clades with more dynamic evolution and many taxon-specific radiations. The dynamically evolving OBPs and CSPs have been hypothesized to function in chemical communication. Intriguingly, we find that seven members of the conserved clades are expressed specifically in the antennae of the clonal raider ant Cerapachys biroi, whereas only one dynamically evolving CSP is antenna specific. The orthologs of the conserved, antenna-specific C. biroi genes are also expressed in antennae of the ants Camponotus floridanus and Harpegnathos saltator, indicating that antenna-specific expression of these OBPs and CSPs is conserved across ants. Most members of the dynamically evolving clades in both protein families are expressed primarily in non-chemosensory tissues and thus likely do not fulfill chemosensory functions.ConclusionsOur results identify candidate OBPs and CSPs that are likely involved in conserved aspects of ant olfaction, and suggest that OBPs and CSPs may not rapidly evolve to recognize species-specific signals.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-718) contains supplementary material, which is available to authorized users.

Molecular identification and expression patterns of odorant binding protein and chemosensory protein genes inAthetis lepigone(Lepidoptera: Noctuidae)

“…Based on the qRT-PCR analyses, we found that 46% of the 28 AlOBP s were highly expressed in the antennae indicating that these AlOBP proteins have putative roles in the odorant reorganization of A. lepigone . Similar to our previous work and to other studies (Gu et al, 2015; McKenzie, Oxley & Kronauer, 2014; Zhang et al, 2016a; Zhang et al, 2013), we found that there were five AlOBP genes highly expressed in non-antennal tissues (legs and wings), including one abdomen-biased AlOBP-encoding gene and four wing-biased AlOBP genes, indicating that these OBPs may have other non-chemosensory functions.…”

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

“…Although a few studies have sought to implicate various small soluble proteins in pheromone recognition (17,(20)(21)(22)(23), it seems more likely that these proteins are involved in generic odorant solubilization and play little role in odor coding (24,25). The only known hymenopteran pheromone ligand-receptor pair to date is the honey bee (Apis mellifera) queen pheromone 9-ODA and the OR AmelOR11 (26).…”

“…The unique spatial arrangement of basiconic sensilla in the clonal raider ant allowed us to examine whether specific odorant receptors were enriched in expression near basiconic sensilla. We therefore analyzed our previously generated sex-specific and tissue-specific RNA-seq libraries (25) and sequenced mRNA isolated specifically from the dorsal and ventral halves of the antennae. To examine phylogenetic influences on gene expression, these data were mapped onto a phylogeny of all putatively functional clonal raider ant odorant receptors (Fig.…”

Genes and genomic processes underpinning the social lives of ants

“…In line with this, the first ant genome projects discovered particularly high number of genes involved in chemical communication, with for example more than 400 putative olfactory receptors in the fire ant [57]. 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].…”