A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon

Okada, Yasukazu; Katsuki, Masako; Okamoto, Naoki; Fujioka, Haruna; Okada, K.

doi:10.1371/journal.pbio.3000541

Cited by 42 publications

(44 citation statements)

References 74 publications

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“…It is tempting to speculate that orthologous genes have similar expression patterns and functions. In related species this is a reasonable hypothesis and the observed expression of aIGFs in cockroaches ( Castro-Arnau et al, 2019 ) and beetles ( Okada et al, 2019 ) is predominantly in the fat body and this seems to be the case for Bombyx aIGF too. What is likely the Rhodnius aIGF is also expressed by the fat body ( Defferrari, Orchard & Lange, 2015 ) as is Drosophila ilp 6 ( Okamoto et al, 2009b ).…”

Section: Discussionmentioning

confidence: 74%

“…In some insects the expression of insulin RTKs have been studied sometimes together with the effects of inactivating one or both insulin RTKs by RNAi ( Wheeler, Buck & Evans, 2006 ; Sang et al, 2016 ; Okada et al, 2019 ). Interestingly, in honeybee larvae that are changed from worker food to royal jelly, that is rich in proteins, it is the RTK A that is upregulated ( Wheeler, Buck & Evans, 2006 ), whereas in two beetle species the effects of RTK inactivation by RNAi is much stronger for type A than for type B ( Sang et al, 2016 ; Okada et al, 2019 ). In the honeybee and the beetle Gnatocerus these receptors have been indirectly linked to an aIGF peptide.…”

Section: Discussionmentioning

confidence: 99%

“…In the beetle Gnatocerus cornutus it has been shown that aIGF specifically stimulates the growth of a sexual ornament ( Okada et al, 2019 ), while higher levels of aIGF are observed in honeybee larvae that are destined to become queens and thus develop functional ovaries ( Wheeler, Buck & Evans, 2006 ). In Gnatocerus aIGF release depends on nutrition status and in honeybees protein rich royal jelly is associated with in increase of aIGF.…”

Section: Discussionmentioning

confidence: 99%

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Arthropod IGF, relaxin and gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Veenstra

2020

PeerJ

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Background Insects have several genes coding for insulin-like peptides and they have been particularly well studied in Drosophila. Some of these hormones function as growth hormones and are produced by the fat body and the brain. These act through a typical insulin receptor tyrosine kinase. Two other Drosophila insulin-like hormones are either known or suspected to act through a G-protein coupled receptor. Although insulin-related peptides are known from other insect species, Drosophila insulin-like peptide 8, one that uses a G-protein coupled receptor, has so far only been identified from Drosophila and other flies. However, its receptor is widespread within arthropods and hence it should have orthologs. Such putative orthologs were recently identified in decapods and have been called gonadulins. Methodology In an effort to identify gonadulins in other arthropods public genome assemblies and short-read archives from insects and other arthropods were explored for the presence of genes and transcripts coding insulin-like peptides and their putative receptors. Results Gonadulins were detected in a number of arthropods. In those species for which transcriptome data from the gonads is available insect gonadulin genes are expressed in the ovaries and at least in some species also in the testes. In some insects differences in gonadulin expression in the ovary between actively reproducing and non-reproducing females differs more than 100-fold. Putative orthologs of Drosophila ilp 6 were also identified. In several non-Dipteran insects these peptides have C-terminally extensions that are alternatively spliced. The predicted peptides have been called arthropod insulin-like growth factors. In cockroaches, termites and stick insects genes coding for the arthropod insulin-like growth factors, gonadulin and relaxin, a third insulin-like peptide, are encoded by genes that are next to one another suggesting that they are the result of a local gene triplication. Such a close chromosomal association was also found for the arthropod insulin-like growth factor and gonadulin genes in spiders. Phylogenetic tree analysis of the typical insulin receptor tyrosine kinases from insects, decapods and chelicerates shows that the insulin signaling pathway evolved differently in these three groups. The G-protein coupled receptors that are related to the Drosophila ilp 8 receptor similarly show significant differences between those groups. Conclusion A local gene triplication in an early ancestor likely yielded three genes coding gonadulin, arthropod insulin-like growth factor and relaxin. Orthologs of these genes are now commonly present in arthropods and almost certainly include the Drosophila insulin-like peptides 6, 7 and 8.

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Section: Discussionmentioning

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Arthropod IGF, relaxin and gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Veenstra

2020

PeerJ

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“…2019; Okada et al. 2019), which would be visible as population‐level shifts in either the slope and/or the intercept of the scaling relationship between horn length and body size (Kawano 1995; Emlen and Nijhout 2000; McCullough et al. 2015).…”

Section: Methodsmentioning

confidence: 99%

Population differences in the strength of sexual selection match relative weapon size in the Japanese rhinoceros beetle,Trypoxylus dichotomus(Coleoptera: Scarabaeidae)†

et al. 2020

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Exaggerated weapons of sexual selection often diverge more rapidly and dramatically than other body parts, suggesting that relevant agents of selection may be discernible in contemporary populations. We examined the ecology, reproductive behavior, and strength of sexual selection on horn length in five recently diverged rhinoceros beetle (Trypoxylus dichotomus) populations that differ in relative horn size. Males with longer horns were better at winning fights in all locations, but the link between winning fights and mating success differed such that selection favored large males with long horns at the two long‐horned populations, but was relaxed or nonexistent at the populations with relatively shorter horns. Observations of local habitat conditions and breeding ecology point to shifts in the relative abundance of feeding territories as the most likely cause of population differences in selection on male weapon size in this species. Comparisons of ecological conditions and selection strength across populations offer critical first steps toward meaningfully linking mating system dynamics, selection patterns, and diversity in sexually selected traits.

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“…Such C-terminally extended insulins are present in several insect species and have sometimes been called insulin-like growth factors as they share characteristics with their homonymes (e.g. Defferrari, et al, 2016;Okada et al, 2019).…”

Section: Page 11mentioning

confidence: 99%

Gonadulins, the fourth type of Insulin-related peptides in Decapods

Veenstra

2020

Preprint

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Insulin and related peptides play important roles in the regulation of growth and reproduction. Until recently three different types of insulin-related peptides had been identified from decapod crustaceans. The identification of two novel insulin-related peptides from Sagmariasus verreauxi and Cherax quadricarinatus by Chandler and colleagues (doi: 10.3390/ijms18091832) suggested that there might a fourth type. Publicly available short read archives show that orthologs of these peptides are commonly present in these animals. Most decapods have two genes coding such peptides, but Penaeus species have likely only one and some palaemonids have three. The peptides they encode have been called gonadulins, as they seem consistently expressed by the gonads.Interestingly, expression levels can vary thousand-fold within ovary and testis of Portunus trituberculatus, where gonadulin 1 is expressed by the testis and gonadulin 2 by the ovary.

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A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon

Cited by 42 publications

References 74 publications

Arthropod IGF, relaxin and gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Arthropod IGF, relaxin and gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Population differences in the strength of sexual selection match relative weapon size in the Japanese rhinoceros beetle,Trypoxylus dichotomus(Coleoptera: Scarabaeidae)†

Gonadulins, the fourth type of Insulin-related peptides in Decapods

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