Abstract
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 TGFβ (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 TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.
Highlights
The complex society of eusocial insects includes sterile castes with phenotypes specialized for individual social tasks
In termites, which are distantly related to hymenopteran social insects, there is still no evidence to support the importance of a universal gene network for the evolution of sterile castes, largely because genetic profiles during caste differentiation have not been clarified
Detection of highly expressed genes in the head before the presoldier molt The expression levels of large numbers of genes (14,204/15,876 genes, 89.5% of all genes described in the model OGSv2.2; [8]) were observed by the present RNA-seq data from 3 molting processes (Fig 1A)
Summary
The complex society of eusocial insects includes sterile castes with phenotypes specialized for individual social tasks. In hymenopteran species (bees, ants and wasps), many sociogenomic studies have been conducted in the last decade (reviewed in [1,2]) based on a vast quantity of genomic and transcriptomic information These studies suggested that a co-option of the universal gene network in the solitary ancestor was involved in the evolution of sterile castes [3,4,5,6,7]. In termites, which are distantly related to hymenopteran social insects, there is still no evidence to support the importance of a universal gene network for the evolution of sterile castes, largely because genetic profiles during caste differentiation have not been clarified. One of the most important species for addressing this issue is the damp-wood termite Zootermopsis nevadensis, because genomic and transcriptomic information is available [8], gene function analysis has been successfully applied [9,10,11], and sterile caste differentiation can be observed under natural conditions [9,12] as well as under artificial hormone treatment [10]
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