Abstract
Nestmate discrimination allows social insects to recognize nestmates from non-nestmates using colony-specific chemosensory cues, which typically evoke aggressive behavior toward non-nestmates. Functional analysis of genes associated with nestmate discrimination has been primarily focused on inter-colonial discrimination in Hymenopterans, and parallel studies in termites, however, are grossly lacking. To fill this gap, we investigated the role of two genes, Orco and 5-HTT, associated with chemosensation and neurotransmission respectively, in nestmate discrimination in a highly eusocial subterranean termite, Odontotermes formosanus (Shiraki). We hypothesized that knocking down of these genes will compromise the nestmate recognition and lead to the antagonistic behavior. To test this hypothesis, we carried out (1) an in vivo RNAi to suppress the expression of Orco and 5-HTT, respectively, (2) a validation study to examine the knockdown efficiency, and finally, (3) a behavioral assay to document the phenotypic impacts/behavioral consequences. As expected, the suppression of either of these two genes elevated stress level (e.g., vibrations and retreats), and led to aggressive behaviors (e.g., biting) in O. formosanus workers toward their nestmates, suggesting both Orco and 5-HTT can modulate nestmate discrimination in termites. This research links chemosensation and neurotransmission with nestmate discrimination at the genetic basis, and lays the foundation for functional analyses of nestmate discrimination in termites.
Highlights
Nestmate discrimination is the ability of social insects to recognize colony members using colony-specific recognition cues (Wilson, 1971)
In this study, we investigated the role of two genes, olfactory receptor co-receptor (Orco) and serotonin transporter (5-HTT), associated with chemosensation and neurotransmission respectively, in nestmate discrimination in a highly eusocial subterranean termite, Odontotermes formosanus (Shiraki)
Evolutionary analysis showed that Orco from O. formosanus was clustered with Orco from Z. nevadensis, C. secundus, B. germanica, and the locust Locusta migratoria, while Orco from two ant species (Harpegnathos saltator and Ooceraea biroi) was clustered in a different branch together with Orco from D. melanogaster, the longhorn beetle Anoplophora glabripennis, and the mosquito Anopheles gambiae (Figure 2B)
Summary
Nestmate discrimination is the ability of social insects to recognize colony members using colony-specific recognition cues (Wilson, 1971). Nestmate discrimination plays a crucial role in maintaining the stability of eusocial societies, ensuring that altruistic behaviors are directed only toward related individuals (Wilson, 1971). The olfactory receptor co-receptor (Orco) is highly conserved across insect species (Nakagawa et al, 2012; Zhou et al, 2012), and is considered to form a tetramer which is arranged around specific pore and bound together by a small cytoplasmic anchor domain (Butterwick et al, 2018). Whether disruption of Orco expression can alter the process of nestmate discrimination is still unclear
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