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Endocuticle is involved in caste differentiation of the lower termite.

ABSTRACT: Caste differentiation in termites is one of the most conspicuous examples of facultative polyphenism in animals. It is clear that specific cuticular formation occurs in hard exocuticles during caste differentiation. However, the developmental pattern of the soft endocuticle in the differentiation pathways of castes is unknown. To reveal whether the endocuticle is involved in caste differentiation, we compared the exocuticle and endocuticle thickness of individuals in 2 pathways (nymph line and worker line) of caste differentiation in the termite Reticulitermes aculabialis. The endocuticle protein genes were identified by transcriptome analysis and the expression patterns of these genes were confirmed in caste differentiation. We found that the endocuticle structure showed dynamic changes in 2 pathways, and the first difference in endocuticle structure occurred after larvae differentiation bifurcated into workers and nymphs. The thinning of the endocuticle was a significant event from nymphs developing into alates with the thickest exocuticle and thinnest endocuticle. The thickest endocuticle layers were found in the heads of the workers and the ultrastructure of the endocuticle in the heads was more complex than that in the thorax-abdomens. Six endocuticle protein genes were identified and annotated as endocuticle structural glycoproteins SgAbd-2, SgAbd-9, and Abd-5. The expression levels of endocuticle protein genes changed dramatically during caste development and the expression levels in neotenic reproductives (secondary reproductives) were significantly higher than those in alates (primary reproductives). These results reveal the roles of endocuticles in caste differentiation and adaptation to the environment.

SUBMITTER: Ye C

PROVIDER: S-EPMC8489109 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

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Endocuticle is involved in caste differentiation of the lower termite.

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