Oxytocin‐like signaling in ants influences metabolic gene expression and locomotor activity

Abstract

Ants are emerging model systems to study cellular signaling because distinct castes possess different physiologic phenotypes within the same colony. Here we studied the functionality of inotocin signaling, an insect ortholog of mammalian oxytocin (OT), which was recently discovered in ants. In Lasius ants, we determined that specialization within the colony, seasonal factors, and physiologic conditions down-regulated the expression of the OT-like signaling system. Given this natural variation, we interrogated its function using RNAi knockdowns. Next-generation RNA sequencing of OT-like precursor knock-down ants highlighted its role in the regulation of genes involved in metabolism. Knock-down ants exhibited higher walking activity and increased self-grooming in the brood chamber. We propose that OT-like signaling in ants is important for regulating metabolic processes and locomotion.-Liutkevičiūtė, Z., Gil-Mansilla, E., Eder, T., Casillas-Pérez, B., Di Giglio, M. G., Muratspahić, E., Grebien, F., Rattei, T., Muttenthaler, M., Cremer, S., Gruber, C. W. Oxytocin-like signaling in ants influences metabolic gene expression and locomotor activity.

Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior

“…Thus, since global knockdown of inotocin affects diuresis, although the receptor is confined to the CNS and no processes of the inotocin-producing neurons extend outside the CNS, it was suggested that inotocin regulates neurosecretory cells that produce a diuretic hormone [158]. More recent work has shown that knockdown of inotocin in Lasius ants results in increased locomotor activity, selfgrooming and influenced expression of genes involved in metabolism [253]. Fig.…”

Comparative and Evolutionary Physiology of Vasopressin/ Oxytocin-Type Neuropeptide Signaling in Invertebrates

“…Furthermore, behavioral analysis of ants in which inotocin precursor gene expression had been knocked-down revealed increased locomotor activity and increased self-grooming in the brood chamber. Based on these findings, the authors concluded that inotocin signaling is important for regulation of energy status in association with locomotion and appetite in Lasius neglectus (68).…”

“…Collectively, these findings led the authors to propose that when Camponotus worker ants start foraging, where there is an increased risk of dessication, inotocin signaling acts to stimulate synthesis of protective CHCs. In this context it is interesting that knockdown of inotocin expression in L. neglectus causes increased locomotor activity (68). Thus, inotocin signaling may act at a physiological level to stimulate synthesis of protective CHCs (Camponotus) and at a behavioral level to inhibit locomotor activity (L. neglectus) as integrated adaptive mechanisms to minimize dessication.…”

“…Thus, building upon previous anatomical and physiological studies (52,56), it would be interesting to determine where the inotocin receptor is expressed in locusts as this would provide a basis for an integrative approach to analysis of the physiological roles of VP/OT-type neuropeptide signaling in this species. Furthermore, one of the most intriguing characteristics of VP/OT-type neuropeptide signaling in insects is the highly conserved expression of inotocin in a pair of neurons located in the suboesophageal ganglion, although in some species additional inotocin-expressing neurons are present in the brain (53,64,68,69). This highly restricted pattern of neuronal expression may, at least in part, explain why loss of VP/OT-type neuropeptide signaling has occurred in some insect lineages (including Drosophila).…”

“…Our discovery that asterotocin triggers fictive feeding in the starfish A. rubens is perhaps the most striking evidence obtained from invertebrates, although it is of course noteworthy that actions of asterotocin are indicative of an orexigenic action that contrasts with the anorexigenic action of oxytocin in mammals. Indirect evidence of VP/OT-type signaling regulating feeding and/or digestion includes the expression of VP/OT-type receptors in the digestive system and regions of nervous system that control feeding and/or digestive processes in molluscs (91), annelids (104), nematodes (41) and crustaceans (73,74) and changes in inotocin precursor expression following a starvation period in ants (68). However, further studies are now needed to investigate in more detail the roles of VP/OT-type neuropeptides in feeding/digestion in these and other invertebrate taxa.…”