Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles.
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.
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan ; Department of Entomology, Washington State University, Pullman, Washington, United States of America.
Hiroki
H
Gotoh
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan ; Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, Japan.
Hitoshi
H
Miyakawa
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan ; Ecological Genetics Laboratory, Center for Frontier Research, National Institute of Genetics, Mishima, Shizuoka, Japan.
Asano
A
Ishikawa
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan ; Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan.
Yuki
Y
Ishikawa
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan.
Yasuhiro
Y
Sugime
Division of Biological Sciences, The University of Montana-Missoula, Missoula, Montana, United States of America.
Douglas J
DJ
Emlen
Department of Entomology, Washington State University, Pullman, Washington, United States of America.
Laura C
LC
Lavine
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan.
Toru
T
Miura
D000818:Animals; D001517:Coleoptera / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D004435:Eating / Q000235:genetics*; D019143:Evolution, Molecular; D005260:Female; D018507:Gene Expression Regulation, Developmental; D007605:Juvenile Hormones / Q000235:genetics* / Q000378:metabolism; D007814:Larva / Q000254:growth & development; D008297:Male; D008334:Mandible / Q000254:growth & development; D034622:RNA Interference; D012727:Sex Characteristics; D012733:Sex Differentiation / Q000235:genetics; D015398:Signal Transduction; D014157:Transcription Factors / Q000235:genetics
D007605:Juvenile Hormones; D014157:Transcription Factors