Specialized odorant receptors in social insects that detect cuticular hydrocarbon cues and candidate pheromones

Abstract

Eusocial insects use cuticular hydrocarbons as components of pheromones that mediate social behaviours, such as caste and nestmate recognition, and regulation of reproduction. In ants such as Harpegnathos saltator, the queen produces a pheromone which suppresses the development of workers’ ovaries and if she is removed, workers can transition to a reproductive state known as gamergate. Here we functionally characterize a subfamily of odorant receptors (Ors) with a nine-exon gene structure that have undergone a massive expansion in ants and other eusocial insects. We deorphanize 22 representative members and find they can detect cuticular hydrocarbons from different ant castes, with one (HsOr263) that responds strongly to gamergate extract and a candidate queen pheromone component. After systematic testing with a diverse panel of hydrocarbons, we find that most Harpegnathos saltator Ors are narrowly tuned, suggesting that several receptors must contribute to detection and discrimination of different cuticular hydrocarbons important in mediating eusocial behaviour.

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

“…Further normalizing these responses by subtracting the "no-UAS" (i.e., from parental flies with only Orco-GAL4 containing chromosomes) control response for each hydrocarbon produced only minor changes in the overall results, with 17 of the 18 suprathreshold HsOR/hydrocarbon combinations exceeding the >30 spikes per s threshold (Dataset S1). Most strikingly, 17 of these 18 HsOR-hydrocarbon combinations were for hydrocarbons with a chain length of C28 or longer, suggesting a tuning bias toward longer-chain alkanes, consistent with our observation of odor coding within the nine-exon HsOr subfamily (15). The single exception was HsOr188, which showed a suprathreshold response to C20.…”

“…1A) (8) because these subfamilies are potentially likely to encompass HsOrs with species-specific functionality often associated with pheromones. Within those parameters, preference was given to HsOrs that lie phylogenetically outside of the nine-exon subfamily in light of the functional characterization of 22 members of that HsOr subfamily in a parallel study (15). HsORs were tested against commercially available alkanes and other compounds known to be present on H. saltator cuticle or in exocrine glands and constituents of our in-house chemical screening library that encompass a selection of general odorants across diverse chemical classes that are commonly tested in insect olfactory systems.…”

Genome sequence of the wheat stem sawfly, Cephus cinctus, a primitive hymenopteran and wheat pest, illuminates evolution of hymenopteran chemoreceptors

“…Most remarkably, a single gene (CcinOr69) is at the base of the extremely large 9-exon subfamily, which is particularly highly expanded in ants and mediates perception of their cuticular hydrocarbons of crucial importance to social interactions (Smith et al 2011;Pask et al 2017). Similarly, a small species-specific clade consisting of CcinOr1-9 is at the base of the large-tandem-array subfamily of 61 genes in A. mellifera (Robertson and Wanner 2006) that includes a receptor for the primary queen pheromone substance, AmelOr11 (Wanner et al 2007), a tandem array that has persisted throughout hymenopteran evolution.…”

Plant‐mediated gene silencing of an essential olfactory‐related Gqα gene enhances resistance to grain aphid in common wheat in greenhouse and field

“…A number of proteins are known to be involved in olfaction in insects. Examples of these include the odorant‐binding protein and the olfactory receptor . Aphids respond to the olfactory sensation of pheromones and use these to fix the host location …”

“…Examples of these include the odorant-binding protein and the olfactory receptor. [11][12][13][14][15] Aphids respond to the olfactory sensation of pheromones and use these to fix the host location. 16 G protein-coupled signal transduction systems are important cellular signal transduction pathways.…”