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

Evolutionarily conserved insulin/insulin-like growth factor (IGF) signaling (IIS) has been identified as a major physiological mechanism underlying the nutrient-dependent regulation of sexually selected weapon growth in animals. However, the molecular mechanisms that couple nutritional state with we...

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Main Authors: Yasukazu Okada, Masako Katsuki, Naoki Okamoto, Haruna Fujioka, Kensuke Okada
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-11-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000541
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spelling doaj-2b3f389669f74aba8558882f2c2e44c32021-07-02T21:22:19ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-11-011711e300054110.1371/journal.pbio.3000541A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.Yasukazu OkadaMasako KatsukiNaoki OkamotoHaruna FujiokaKensuke OkadaEvolutionarily conserved insulin/insulin-like growth factor (IGF) signaling (IIS) has been identified as a major physiological mechanism underlying the nutrient-dependent regulation of sexually selected weapon growth in animals. However, the molecular mechanisms that couple nutritional state with weapon growth remain largely unknown. Here, we show that one specific subtype of insulin-like peptide (ILP) responds to nutrient status and thereby regulates weapon size in the broad-horned flour beetle Gnatocerus cornutus. By using transcriptome information, we identified five G. cornutus ILP (GcorILP1-5) and two G. cornutus insulin-like receptor (GcorInR1, -2) genes in the G. cornutus genome. RNA interference (RNAi)-mediated gene silencing revealed that a certain subtype of ILP, GcorILP2, specifically regulated weapon size. Importantly, GcorILP2 was highly and specifically expressed in the fat body in a condition-dependent manner. We further found that GcorInR1 and GcorInR2 are functionally redundant but that the latter is partially specialized for regulating weapon growth. These results strongly suggest that GcorILP2 is an important component of the developmental mechanism that couples nutritional state to weapon growth in G. cornutus. We propose that the duplication and subsequent diversification of IIS genes played a pivotal role in the evolution of the complex growth regulation of secondary sexual traits.https://doi.org/10.1371/journal.pbio.3000541
collection DOAJ
language English
format Article
sources DOAJ
author Yasukazu Okada
Masako Katsuki
Naoki Okamoto
Haruna Fujioka
Kensuke Okada
spellingShingle Yasukazu Okada
Masako Katsuki
Naoki Okamoto
Haruna Fujioka
Kensuke Okada
A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
PLoS Biology
author_facet Yasukazu Okada
Masako Katsuki
Naoki Okamoto
Haruna Fujioka
Kensuke Okada
author_sort Yasukazu Okada
title A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
title_short A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
title_full A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
title_fullStr A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
title_full_unstemmed A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
title_sort specific type of insulin-like peptide regulates the conditional growth of a beetle weapon.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2019-11-01
description Evolutionarily conserved insulin/insulin-like growth factor (IGF) signaling (IIS) has been identified as a major physiological mechanism underlying the nutrient-dependent regulation of sexually selected weapon growth in animals. However, the molecular mechanisms that couple nutritional state with weapon growth remain largely unknown. Here, we show that one specific subtype of insulin-like peptide (ILP) responds to nutrient status and thereby regulates weapon size in the broad-horned flour beetle Gnatocerus cornutus. By using transcriptome information, we identified five G. cornutus ILP (GcorILP1-5) and two G. cornutus insulin-like receptor (GcorInR1, -2) genes in the G. cornutus genome. RNA interference (RNAi)-mediated gene silencing revealed that a certain subtype of ILP, GcorILP2, specifically regulated weapon size. Importantly, GcorILP2 was highly and specifically expressed in the fat body in a condition-dependent manner. We further found that GcorInR1 and GcorInR2 are functionally redundant but that the latter is partially specialized for regulating weapon growth. These results strongly suggest that GcorILP2 is an important component of the developmental mechanism that couples nutritional state to weapon growth in G. cornutus. We propose that the duplication and subsequent diversification of IIS genes played a pivotal role in the evolution of the complex growth regulation of secondary sexual traits.
url https://doi.org/10.1371/journal.pbio.3000541
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