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

Abstract

A major aim of sociogenomic research is to uncover common principles in the molecular evolution of sociality. This endeavor has been hampered by the small number of specific genes currently known to function in social behavior. Here we provide several lines of evidence suggesting that ants have evolved a large and novel clade of odorant receptor (OR) genes to perceive hydrocarbonbased pheromones, arguably the most important signals in ant communication. This genomic expansion is also mirrored in the ant brain via a corresponding expansion of a specific cluster of glomeruli in the antennal lobe. We show that in the clonal raider ant, hydrocarbon-sensitive basiconic sensilla are found only on the ventral surface of the female antennal club. Correspondingly, nearly all genes in a clade of 180 ORs within the 9-exon subfamily of ORs are expressed exclusively in females and are highly enriched in expression in the ventral half of the antennal club. Furthermore, we found that across species and sexes, the number of 9-exon ORs expressed in antennae is tightly correlated with the number of glomeruli in the antennal lobe region innervated by odorant receptor neurons from basiconic sensilla. Evolutionary analyses show that this clade underwent a striking gene expansion in the ancestors of all ants and slower but continued expansion in extant ant lineages. This evidence suggests that ants have evolved a large clade of genes to support pheromone perception and that gene duplications have played an important role in the molecular evolution of ant communication.sociogenomics | chemosensation | social evolution | antennal lobe | Formicidae T he field of sociogenomics seeks to understand the molecular basis of sociality, asking how social life evolved and how it is governed at the genomic level (1). A particularly pertinent question in the field is the role of novel genes vs. conserved genes in the evolution and regulation of social behaviors, including communication (2, 3). Communication is important to a broad range of organisms, yet relatively little is known about the genetic components of communication systems and how they evolve. A particularly interesting question in the field is how social signals are perceived and what sort of genetic and physiological specializations facilitate signal perception in highly social organisms (4, 5). In the most tractable sociogenomic models, the eusocial hymenopteran insects, communication is largely chemical, and the genetics and physiology of chemosensation in these species may hold the key to understanding their advanced communication (4,6, 74).Much is already known about the insect chemosensory system in general (8,9). Briefly, chemicals are detected by porous sensory hairs (sensilla) located on chemosensory organs such as the legs, wings, palps, and especially the antennae. The sensilla house the dendrites of olfactory and/or gustatory receptor neurons (ORNs/GRNs) with receptor proteins in the olfactory receptor (OR), the gustatory receptor (GR), or the ionotropic receptor (IR) gene ...

Functional characterization of odorant receptors in the ponerine ant, Harpegnathos saltator

“…Nevertheless, this broader analysis further supports and indeed extends our observation that HsOR-mediated responses to hydrocarbons are not, as previously hypothesized (8,9,14), restricted to the nine-exon HsOr gene subfamily. Furthermore, within the subset of statistically significant responses, we discovered a strong bias toward the longer chain alkanes commonly found in H. saltator CHCs (5, 18).…”

“…Previous work has strongly implicated the nine-exon subfamily of ORs, which makes up nearly 30% of the 347 putative Or genes in H. saltator genome (HsOrs) and is highly expanded within the ant lineage (8,9), in the detection of CHCs, based on their enrichment along the hydrocarbon-sensitive ventral portion of the worker antennae (14). Transgenic expression of a subset of these genes in Drosophila olfactory sensilla confers receptor-specific responses to a panel of CHCs.…”

“…These hydrocarbons were initially used to test responses from the two nine-exon HsORs in our receptor collection, which, based on phylogenetic and transcriptomic considerations, is hypothesized to be the HsOr gene subfamily most likely to detect CHC pheromones involved in eusociality (8,9,14). Of these receptors, HsOr271 displayed a strong response (60 spikes per s, Fig.…”

orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants

“…In Drosophila , pheromone receptors have been identified that belong to multiple insect chemosensory receptor families, including odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), and pickpocket channels (PPKs) (Kohl et al, 2015). Ants have numbers of GRs, IRs, and PPKs that are typical for insects, while their OR repertoire is highly expanded (McKenzie et al, 2016; Oxley et al, 2014; Smith et al, 2011a, 2011b; Zhou et al, 2012) (Figure 1A and Table S1). This raises the possibility that the expansion of ORs specifically, rather than chemoreceptors in general, may underlie the evolution of complex chemical communication in ants.…”

“…This raises the possibility that the expansion of ORs specifically, rather than chemoreceptors in general, may underlie the evolution of complex chemical communication in ants. Ants also have exceedingly large numbers of glomeruli in their antennal lobes, which likely mirror their expanded OR gene repertoire (McKenzie et al, 2016; Zube et al, 2008) (Table S1). Insect ORs function as chemosensory receptors by dimerizing with the highly-conserved co-receptor protein Orco to form ligand-gated ion channels (Jones et al, 2005; Larsson et al, 2004; Sato et al, 2008).…”