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Dopamine regulates termite soldier differentiation through trophallactic behaviours.

ABSTRACT: Caste polyphenism in social insects is regulated by social interactions among colony members. Trophallaxis is one of the most frequently observed interactions, but no studies have been conducted identifying the intrinsic factors involved in this behaviour and caste differentiation. Dopamine (DA) has multiple roles in the modulation of behaviours and physiology, and it produces species-specific behaviours in animals. Here, to verify the role of DA in termite soldier differentiation, we focused on the first soldier in an incipient colony of Zootermopsis nevadensis, which always differentiates from the oldest 3rd instar (No. 1 larva) via a presoldier. First, brain DA levels of the No. 1 larva at day 3 after its appearance were significantly higher than day 0. Second, DA synthesis gene expression levels were extraordinarily high in the No. 1 larva at day 0-1 after appearance. Finally, injection of a DA receptor antagonist into the No. 1 larva resulted in the inhibition of presoldier differentiation. Behavioural observations of the antagonist or control-injected larvae suggested that brain DA and signalling activity regulate the frequencies of trophallaxis from reproductives and presoldier differentiation. Because trophallaxis is a social behaviour frequently observed in natural conditions, the role of DA should be investigated in other social insects with frequent trophallactic and allogrooming behaviour.

SUBMITTER: Yaguchi H

PROVIDER: S-EPMC4785978 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Dopamine regulates termite soldier differentiation through trophallactic behaviours.

Yaguchi Hajime H Inoue Takaya T Sasaki Ken K Maekawa Kiyoto K

Royal Society open science 20160210 2

Caste polyphenism in social insects is regulated by social interactions among colony members. Trophallaxis is one of the most frequently observed interactions, but no studies have been conducted identifying the intrinsic factors involved in this behaviour and caste differentiation. Dopamine (DA) has multiple roles in the modulation of behaviours and physiology, and it produces species-specific behaviours in animals. Here, to verify the role of DA in termite soldier differentiation, we focused on ...[more]

PMID: 26998327

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Project description:A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGF? (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGF? signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.

Dataset Information

Dopamine regulates termite soldier differentiation through trophallactic behaviours.

Publications

Dopamine regulates termite soldier differentiation through trophallactic behaviours.

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