Multi-functional roles of a soldier-specific volatile as a worker arrestant, primer pheromone and an antimicrobial agent in a termite

Abstract

Division of labour in eusocial insects is characterized by efficient communication systems based on pheromones. Among such insects, termites have evolved specialized sterile defenders, called soldiers. Because they are incapable of feeding themselves, it has been suggested that soldiers are sustained by workers and emit the pheromone arresting workers. However, such a soldier pheromone has not been identified in any termite species, and the details of the soldier-worker interaction remain to be explored. Here, we identified a soldier-specific volatile sesquiterpene as a worker arrestant, which also acts as a primer pheromone regulating soldier differentiation and fungistatic agent in a termite Chemical analyses revealed that (-)--elemene is the major component of soldier extract, and its authentic standard exhibited arrestant activity to workers and inhibited the differentiation from workers to soldiers. This compound also showed fungistatic activity against entomopathogenic fungi. These suggest that (-)--elemene secreted by soldiers acts not only as a worker arrestant but also as one component of inhibitory primer pheromone and an anti-pathogenic agent. Our study provides novel evidence supporting the multi-functionality of termite soldier pheromone and provides new insights into the role of soldiers and the evolutionary mechanisms of pheromone compounds.

Transcriptomic changes during caste development through social interactions in the termite Zootermopsis nevadensis

“…Soldiers are differentiated from workers via an intermediate presoldier stage. The new production of soldiers is promoted by the presence of reproductives (Bordereau & Han, ; Maekawa, Nakamura, & Watanabe, ) and suppressed by existing soldiers (Mitaka, Mori, & Matsuura, ; Watanabe, Gotoh, Miura, & Maekawa, ). Caste differentiation is generally determined in an environmentally sensitive period during postembryonic development, probably by pheromonal substrates transmitted via inter‐individual interactions (Noirot, ; Watanabe, Gotoh, Miura, & Maekawa, ).…”

Termite soldiers contribute to social immunity by synthesizing potent oral secretions

“…Previous studies exploring the antimicrobial activity of soldier‐derived secretions focused on species that are distantly related to Ma. darwiniensis (Rosengaus et al ., ; Fuller, ; Mitaka et al ., ). The occurrence of antimicrobial activity in diverse termite lineages therefore raises the possibility that an immune role for soldiers is a conserved ancestral termite trait.…”

“…For example, GNBP2 is known to have direct antimicrobial properties (Bulmer et al ., ). However, evidence also shows that insect‐ (including termite) secreted chemicals can possess antimicrobial activity (Rosengaus et al ., ; Otti et al ., ; Mitaka et al ., ). Chemically mediated microbial inhibition, perhaps via benzoquinone, could therefore play a significant role in the inhibition we observed in Ma.…”

“…Some evidence from both termites and other soldier‐first societies such as thrips (Turnbull et al ., ) indicates that soldiers can contribute to colony‐level immunity (Rosengaus et al ., ; Fuller ; Gao & Thompson ; Negulescu et al ., ; Mitaka et al ., ). However, most investigations into social immunity have been conducted in workers, where a large number of mechanisms have been shown to protect social insect colonies against pathogen exposure (Cremer et al ., ; Hamilton et al ., ; Stroeymeyt et al ., ; Meunier ; Vannette et al ., ; Wang et al ., ).…”

Volatile Terpenes and Terpenoids from Workers and Queens of Monomorium chinense (Hymenoptera: Formicidae)

“…For example, β-elemene was detected in termite Reticulitermes speratus (Isoptera: Rhinotermitidae), δ-elemene, γ-curcumene, β-cedrene, β-himachalene, and β-acoradiene in butterflies (Lepidoptera: Papilionidae), β-sesquiphellandrene in stinkbugs Thyanta pallidovirens and Piezodorus guildinii (Hemiptera: Pentatomidae), and β-curcumene in ciid beetles Octotemnus glabriculus and Cis boleti (Coleoptera: Ciidae). Terpenes play multiple functions in these insects, serving as inhibitory primer pheromones, queen-recognition and sex pheromones, defensive chemicals against natural enemies, and antimicrobials against pathogens [ 29 , 30 , 31 , 32 , 33 , 34 ]. Further research is needed to determine whether terpenes and terpenoids play similar roles in M. chinense.…”