Abstract
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.
Highlights
The evolution of sex-specific traits in animals has long fascinated biologists
Developmental mechanisms generating sexspecific trait growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures of sexual selection
We examined the regulation and function of a key sex determination gene in animals, doublesex, and its interaction with juvenile hormone (JH), an important insect hormone known to regulate insect polyphenisms including the regulation of the disproportionate growth of male stag beetle mandibles
Summary
Sexual dimorphisms are widespread across diverse animal taxa and include exaggerated sexually selected traits like the antlers of deer, the enormous clawed chelae of crabs, and the elaborate trains of peacocks [1], [2], [3]. Developmental mechanisms generating sexspecific trait growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures of sexual selection. The near universality of sex differences in the nutrition sensitivity of these traits suggests that common developmental mechanisms may be involved. We still know almost nothing about how the processes of sex-specific growth and nutrition-sensitivity interact with each other to generate sexual dimorphism
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