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

Abstract

Animals use a variety of sensory modalities-including visual, acoustic, and chemical-to sense their environment and interact with both conspecifics and other species. Such communication is especially critical in eusocial insects such as honey bees and ants, where cooperation is critical for survival and reproductive success. Various classes of chemoreceptors have been hypothesized to play essential roles in the origin and evolution of eusociality in ants, through their functional roles in pheromone detection that characterizes reproductive status and colony membership. To better understand the molecular mechanisms by which chemoreceptors regulate social behaviors, we investigated the roles of a critical class of chemoreceptors, the odorant receptors (ORs), from the ponerine ant Harpegnathos saltator in detecting cuticular hydrocarbon pheromones. In light of the massive OR expansion in ants (∼400 genes per species), a representative survey based on phylogenetic and transcriptomic criteria was carried out across discrete odorant receptor subfamilies. Responses to several classes of semiochemicals are described, including cuticular hydrocarbons and mandibular gland components that act as H. saltator pheromones, and a range of more traditional general odorants. When viewed through the prism of caste-specific OR enrichment and distinctive OR subfamily odorant response profiles, our findings suggest that whereas individual HsOrs appear to be narrowly tuned, there is no apparent segregation of tuning responses within any discrete HsOr subfamily. Instead, the HsOR gene family as a whole responds to a broad array of compounds, including both cuticular hydrocarbons and general odorants that are likely to mediate distinct behaviors.ant | odorant receptor | odor coding | pheromone T he detection of ecologically relevant chemosensory information is critical to the survival and propagation of all organisms. For example, sex pheromones allow members of the same species to locate and assess mates, and predators use volatile kairomones to locate prey. There is long-standing interest in understanding the pheromonal communication of insects and, in particular, exploring how semiochemicals govern the interactions of eusocial colonies. Ants are intriguing for the purposes of chemosensory studies, because of their diversity and exploitation of cuticular hydrocarbons (CHCs) for nest-mate recognition, and as signals of reproductive and caste status. Most ants live in closed societies within a shared colony or nest-with stereotypic social behaviors that involve a strict division of reproductive labor-in which multiple overlapping generations of sterile workers cooperate to nurture the progeny produced by the reproductives, which usually consist of single or small numbers of long-lived, highly fertile queens and short-lived male drones (1). Reproductive status within the colony is thought to be signaled primarily by a subset of the hydrocarbons secreted onto the external cuticle of insects and other arthropods (e.g. ref.2) that also func...

The diversity and evolution of odorant receptors in beetles (Coleoptera)

“…The enormous diversity of ORs (and potential ligands) has in turn hampered their functional characterization, especially in nonmodel species. Ligands have been described for most of the ORs in Drosophila melanogaster Meigen (Mansourian and Stensmyr, 2015), and relatively large subsets of ORs have been functionally characterized from a few other insects (Wang et al, 2010;de Fouchier et al, 2017;Liu et al, 2017;Slone et al, 2017). Otherwise, function is broadly known only for the pheromone receptors of the Lepidoptera (Zhang and Löfstedt, 2015;Yuvaraj et al, 2018) and a few ORs from other scattered insect species (eg Mitchell et al, 2012;Andersson et al, 2016;Miyazaki et al, 2018).…”

Hydrocarbons mediate seed dispersal: a new mechanism of vespicochory

“…Myrmecochory is therefore a key evolutionary innovation and a globally important driver of plant diversity (Lengyel et al, 2010). Recent studies indicate that cuticular hydrocarbons act as chemical communication cues in the olfactory system of ants (Martin & Drijfhout, 2009;Sturgis & Gordon, 2012;Slone et al, 2017). Gustatory cues from elaiosomes of typical myrmecochorous plants were similar to those from the haemolymph of the typical insect prey of ants (Hughes et al, 1994;Gammans et al, 2005;Fischer et al, 2008).…”

Odor Coding of Nestmate Recognition in the Eusocial AntCamponotus floridanus

“…Insect ORs are expressed in olfactory receptor neurons (ORNs) housed within sensilla on the antennae (reviewed in (22)), where they function as heteromeric complexes consisting of an obligate and conserved OR co-receptor (Orco) and at least one “tuning” OR that determines odorant (ligand) specificity (23-29). Several studies have revealed a large expansion of the OR gene family in ants as well as other eusocial insects (23, 30-37), leading to the demonstration that this expanded chemoreceptor family is responsible for the detection of socially relevant chemical cues such as CHCs (38, 39).…”