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

Abstract

One of the most striking examples of phenotypic plasticity is the different phenotypes (i.e., castes) within a same nest of social insects. Castes usually derive from a single genotype initially by receiving social cues among individuals during development. Specific gene expression changes may be involved in caste differentiation, and thus, the regulatory mechanism of these changes should be clarified in order to understand social maintenance and evolution. The damp‐wood termite Zootermopsis nevadensis is one of the most important model termite species, due to not only the availability of genomic, transcriptomic, and epigenomic information but also evidence that soldier‐ and worker‐destined individuals can be identified in natural conditions. Given that the nutritional intakes via social interactions are crucial for caste differentiation in this species, there is a possibility that transcriptomic changes are influenced by the nutritional difference among these individuals. Here, whole body RNA‐seq analysis of 3rd‐instar larvae with biological replications and Gene Ontology and Kyoto Encyclopedia of Genes and Genomes enrichment analyses were conducted. We found the drastic expression differences during caste developments between soldier‐ and worker‐destined individuals. The results indicated that there are several key signaling pathways responsible for caste formations, which are involved in developments and social interactions. Particularly, the nutritional sensitive signaling was upregulated in soldier‐destined individuals, while some metabolic pathways were identified in worker‐destined individuals. These bioinformatic data obtained should be utilized to examine the molecular mechanisms of caste determination in social insects.

Methoprene-Induced Genes in Workers of Formosan Subterranean Termites (Coptotermes formosanus Shiraki)

“…After topical application of JHA on pseudergates of H. sjostedti, the JH titer decreased at first, but gradually increased and reached the plateau just before the pseudergate-presoldier molt [5]. According to our RNA-Seq results, the JH synthesis pathway is the most significantly enriched pathway, which was consistent with the RNA-Seq study in Z. nevadensis [42]. The changes of expression profiles of the JH synthesis genes were also documented in Z. nevadensis [43].…”

“…The upregulation of those metabolic pathways reflected the histological change after the application of JHA. The enrichment of metabolic pathways was also reported in Z. nevadensis [42]. The fat body plays an important role in insect metamorphosis.…”

“…20-hydroxyecdysone (20E) signaling pathway is required for the accomplishment of molting. Expression of ecdysone synthesis genes increases three days after the appearance of the first instar larvae in Z. nevadensis [42]. It takes around eight days for the first appearing third instar larvae to molt into a presoldier [49], but at least ten days for the artificial induction of presoldiers in C. formosanus [25].…”

The making of the defensive caste: Physiology, development, and evolution of the soldier differentiation in termites

“…In phenotypic plasticity in insects, some studies suggested the interconnection between insulin and Hippo/Toll pathways (Cassa & Moczek, 2018; Gotoh et al, 2015). In an incipient colony of Z. nevadensis , KEGG analysis showed that the Hippo pathway was upregulated in the first offspring individual that becomes the first soldier (Yaguchi, Suzuki, Matsunami, Shigenobu, & Maekawa, 2019). Taken together, there should be some crosstalks among JH, ecdysone, insulin, and other physiological signaling pathways including Hippo/Toll pathway, and the coordination of these pathways is suggested to determine caste fates, leading to the expressions of caste‐specific phenotypes.…”

Comparison of gene expression profiles among caste differentiations in the termite Reticulitermes speratus

“…Some important genes, such as hexamerin 8 , insulin receptor 12 , distal-less 9 and deformed 13 , 14 have been found to be specifically expressed at a certain point during the molting period (i.e., worker-presoldier molt). Furthermore, some specifically expressed genes and cascades have been identified during the differentiation of the first soldier in an incipient colony 15 – 17 , based on the genome sequences of the primitive termite Zootermopsis nevadensis 18 . However, even in Z. nevadensis, there are no artificial induction methods of caste differentiation other than those for soldiers, therefore, comprehensive gene expression patterns and comparative transcriptome profiles among caste differentiations are not fully understood.…”