Dataset Information

Juvenile hormone regulates extreme mandible growth in male stag beetles.

ABSTRACT: The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.

SUBMITTER: Gotoh H

PROVIDER: S-EPMC3120829 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Juvenile hormone regulates extreme mandible growth in male stag beetles.

Gotoh Hiroki H Cornette Richard R Koshikawa Shigeyuki S Okada Yasukazu Y Lavine Laura Corley LC Emlen Douglas J DJ Miura Toru T

PloS one 20110622 6

The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with othe ...[more]

PMID: 21731659

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Project description:Sexual dimorphisms in trait expression are widespread among animals and are especially pronounced in ornaments and weapons of sexual selection, which can attain exaggerated sizes. Expression of exaggerated traits is usually male-specific and nutrition sensitive. Consequently, the developmental mechanisms generating sexually dimorphic growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures. Yet we know little about how either of these mechanisms work, much less how they might interact with each other. We investigated the developmental mechanisms of sex-specific mandible growth in the stag beetle Cyclommatus metallifer, focusing on doublesex gene function and its interaction with juvenile hormone (JH) signaling. doublesex genes encode transcription factors that orchestrate male and female specific trait development, and JH acts as a mediator between nutrition and mandible growth. We found that the Cmdsx gene regulates sex differentiation in the stag beetle. Knockdown of Cmdsx by RNA-interference in both males and females produced intersex phenotypes, indicating a role for Cmdsx in sex-specific trait growth. By combining knockdown of Cmdsx with JH treatment, we showed that female-specific splice variants of Cmdsx contribute to the insensitivity of female mandibles to JH: knockdown of Cmdsx reversed this pattern, so that mandibles in knockdown females were stimulated to grow by JH treatment. In contrast, mandibles in knockdown males retained some sensitivity to JH, though mandibles in these individuals did not attain the full sizes of wild type males. We suggest that moderate JH sensitivity of mandibular cells may be the default developmental state for both sexes, with sex-specific Dsx protein decreasing sensitivity in females, and increasing it in males. This study is the first to demonstrate a causal link between the sex determination and JH signaling pathways, which clearly interact to determine the developmental fates and final sizes of nutrition-dependent secondary-sexual characters.

Project description:Adult females of stag beetles (Coleoptera: Lucanidae) possess an ovipositor-associated mycangium for conveying symbiotic microorganisms. In most lucanid species, their mycangium contains yeast symbionts of the genus Scheffersomyces Kurtzman and Suzuki that are known for their xylose-fermenting capability. The lucanid genus Platycerus Geoffroy, 1762 is a group of small blue stag beetles, in which ten Japanese species constitute a monophyletic clade. Here we examined the evolutionary relationships of these Japanese Platycerus species and their yeast symbionts, together with a Korean Platycerus species and other lucanid species as outgroup taxa. Based on the internal transcribed spacer (ITS) and the intergenic spacer (IGS) sequences, the yeast symbionts of all Platycerus species were closely related to each other and formed a monophyletic clade. There is no variation in ITS sequences of the yeast symbionts of the Japanese Platycerus species. Based on IGS sequences, the yeast symbionts formed clusters that largely reflected the geographic distribution of the host insects, being shared by sympatric Platycerus species except for P. delicatulus Lewis, 1883 and P. viridicuprus Kubota & Otobe, The symbiont phylogeny was globally not congruent with the host COI-based phylogeny, although some local congruences were observed. Statistically significant correlations were detected between the genetic distances of COI sequences of the host insects and those of IGS sequences of the yeast symbionts in Japan. These results suggest that, at least to some extent, the host insects and the yeast symbionts may have experienced co-evolutionary associations. While the Japanese Platycerus species formed a monophyletic clade in the COI phylogeny, the yeast symbionts of Japanese P. viridicuprus were very closely related to those of Korean P. hongwonpyoi Imura & Choe, 1989, suggesting the possibility that a recent secondary contact of the two beetle species during a marine withdrawal, e.g., in the last glacial period, might have resulted in an inter-specific horizontal transmission of the yeast symbiont.

Dataset Information

Juvenile hormone regulates extreme mandible growth in male stag beetles.

Publications

Juvenile hormone regulates extreme mandible growth in male stag beetles.

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