Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Abstract

Background. Insulin-like growth factor (IGF) and other Insulin-like peptides (ilps) are important hormones regulating growth and development in animals. Whereas most animals have a single female and male adult phenotype, in some insect species the same genome may lead to different final forms. Perhaps the best known example is the honeybee where females can either develop into queens or workers. More extreme forms of such polyphenism occur in termites, where queens, kings, workers and soldiers coexist. Both juvenile hormone and insulin-like peptides are known to regulate growth and reproduction as well as polyphenism. In termites the role of juvenile hormone in reproduction and the induction of the soldier caste is well known, but the role of IGF and other ilps in these processes remains largely unknown. Here the various termite ilps are identified and hypotheses regarding their functions suggested. Methods. Genome assemblies and transcriptome short read archives (SRAs) were used to identify insulin-like peptides and neuropeptides in termites and to determine their expression in different species, tissues and castes. Results and Discussion. Termites have seven different ilps, i.e. gonadulin, IGF and an ortholog of Drosophila insulin-like peptide 7 (dilp7), which are commonly present in insects, and four smaller peptides, that have collectively been called short IGF-related peptides (sirps) and individually atirpin, birpin, cirpin and brovirpin. Gonadulin is lost from the higher termites which have however amplified the brovirpin gene, of which they often have two or three paralogs. Based on differential expression of these genes it seems likely that IGF is a growth hormone and atirpin an autocrine tissue factor that is released when a tissue faces metabolic stress. Birpin seems to be responsible for growth and in the absence of juvenile hormone this may lead to reproductive adults or, when juvenile hormone is present, to soldiers. Brovirpin is expressed both by the brain and the ovary and likely stimulates vitellogenesis, while the function of cirpin is less clear.

Different neuroendocrine cell types in thepars intercerebralisofPeriplaneta americanaproduce their own specific IGF-related peptides

“…Termites have three different insulin/IGF RTKs and four different sirps, of which one, like Periplaneta sirp-5, is expressed in multiple tissues, while the other three are probably expressed by brain neuroendocrine cells. Interestingly, one of latter is also expressed by the ovary (Veenstra, 2023), just like Periplaneta sirp-3.…”

“…The big question is of course, why there are so many different sirp expressing cell types and how do their functions differ ? Periplaneta is closely related to termites − which are social cockroaches − and similarities between termites and the American cockroach are thus not surprising (Veenstra, 2023). Termites have three different insulin/IGF RTKs and four different sirps, of which one, like Periplaneta sirp-5, is expressed in multiple tissues, while the other three are probably expressed by brain neuroendocrine cells.…”

“…It is possible that the third termite sirpin would be used by workers to stimulate protein synthesis in the salivary gland, but evidence in support of the latter function is very weak at best. Expression of IGF in termites seems to increase during body growth associated with physogastry that is so prominent in females of the macrotermitidae (Veenstra, 2023).…”

“…The term insulin-like peptide and its acronym ilp does not differentiate between these smaller peptides and the triplet consisting of IGF, gonadulin and the dilp7 orthologs. I have therefore proposed to call these smaller peptides short IGF-related peptides (sirps) to make this distinction (Veenstra, 2023). Although sirps are likely descendants of IGF, they are prone to have different functions in different species.…”