Molecular characterization and expression variation of the odorant receptor co-receptor in the Formosan subterranean termite

Abstract

Subterranean termites live in underground colonies with a division of labor among castes (i.e., queens and kings, workers, and soldiers). The function of social colonies relies on sophisticated chemical communication. Olfaction, the sense of smell from food, pathogens, and colony members, plays an important role in their social life. Olfactory plasticity in insects can be induced by long- and short-term environmental perturbations, allowing adaptive responses to the chemical environment according to their physiological and behavioral state. However, there is a paucity of information on the molecular basis of olfaction in termites. In this study, we identified an ortholog encoding the odorant receptor co-receptor (Orco) in the Formosan subterranean termite, Coptotermes formosanus, and examined its expression variation across developmental stages and in response to social conditions. We found that C. formosanus Orco showed conserved sequence and structure compared with other insects. Spatial and temporal analyses showed that the Orco gene was primarily expressed in the antennae, and it was expressed in eggs and all postembryonic developmental stages. The antennal expression of Orco was upregulated in alates (winged reproductives) compared with workers and soldiers. Further, the expression of Orco decreased in workers after starvation for seven days, but it was not affected by the absence of soldiers or different group sizes. Our study reveals the molecular characteristics of Orco in a termite, and the results suggest a link between olfactory sensitivity and nutritional status. Further studies are warranted to better understand the role of Orco in olfactory plasticity and behavioral response.

Identification of the trail-following pheromone receptor in termites

“…In contrast to eusocial Hymenoptera, the molecular aspects of termite chemical communication and orientation remain largely understudied despite the systematic effort previously dedicated to unveil the chemical identity, glandular origin and biological functions of termite pheromones (Bagnères & Hanus, 2015;Bordereau & Pasteels, 2011;Mitaka & Akino, 2021;Sillam-Dussès, 2010). Current knowledge is limited to a few studies listing the termite OR repertoire (Harrison et al, 2018;Johny et al, 2023;Terrapon et al, 2014), caste-specific OR expression (Mitaka et al, 2016), or addressing the significance of ORCo for olfactory function (Castillo et al, 2022;Gao et al, 2020). Multiple evidence suggests that the complex communication and orientation demands in the colonies of eusocial Hymenoptera are facilitated by the greatly expanded repertoire of ORs, especially that of the 9-exon subfamily in ants and paper wasps participating in the detection of cuticular hydrocarbons (CHCs) as important cues in contact chemoreception of colony and caste identity and fertility status in eusocial insects (Engsontia et al, 2015;Legan et al, 2021;McKenzie et al, 2016;Pask et al, 2017;Zhou et al, 2015).…”

Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants

“…Among the OR genes overexpressed in nurses was also the co-receptor Orco , which is widely expressed in olfactory sensory neurons and nearly unchanged in sequence in distant insect taxa 120 – 122 . ORs form a unique class of heteromeric cation channels composed of two related heptahelical subunits: a divergent OR subunit that confers odor specificity, and the co-receptor Orco subunit 123 , 124 . Since those functional receptors would increase the sensitivity of the workers to odors, we propose that the overexpression of Orco may indicate higher olfactory sensitivity to odors in the antennae of nurses compared to foragers.…”

Chemical predation signals: a possible major influence on the differential predation strategy of ants on termites

“…Field experimental studies on the interactions between the two populations have never been interrupted, in which the effect of predators on the population size of prey has been a hot research topic 1,3 . In nature, most trophic-level relationships exist in the form of predator-prey relationships, and the balance of ecosystems is largely determined by the balance of predator-prey relationships 4 .…”