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      Developmental Link between Sex and Nutrition; doublesex Regulates Sex-Specific Mandible Growth via Juvenile Hormone Signaling in Stag Beetles

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          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.

          Author Summary

          Sexual dimorphisms such as the exaggerated antlers of deer, the enormous clawed chelae of crabs, and the horns and mandibles of beetles, are widespread across animal taxa and have fascinated biologists for centuries. Much recent work has uncovered the importance of the role of the sex-determination pathway in the expression of sexually dimorphic traits. However, critical interactions between this pathway and other growth regulatory mechanisms – for example, the physiological mechanisms involved in nutrition-dependent expression of these traits – are less well understood. In this study, we provide evidence of a developmental link between nutrition-sensitivity and sexual differentiation in the giant mandibles of the sexually dimorphic stag beetle, Cyclommatus metallifer. We examined the regulation and function of a key sex determination gene in animals, doublesex ( dsx), 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. We found that Cmdsx changes mandibular responsiveness to JH in a sex-specific pattern. Based on these results, we hypothesize that sex-specific regulation of JH responsiveness is a developmental link between nutrition and sexual differentiation in stag beetles.

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          Most cited references24

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          A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons.

          Many male animals wield ornaments or weapons of exaggerated proportions. We propose that increased cellular sensitivity to signaling through the insulin/insulin-like growth factor (IGF) pathway may be responsible for the extreme growth of these structures. We document how rhinoceros beetle horns, a sexually selected weapon, are more sensitive to nutrition and more responsive to perturbation of the insulin/IGF pathway than other body structures. We then illustrate how enhanced sensitivity to insulin/IGF signaling in a growing ornament or weapon would cause heightened condition sensitivity and increased variability in expression among individuals--critical properties of reliable signals of male quality. The possibility that reliable signaling arises as a by-product of the growth mechanism may explain why trait exaggeration has evolved so many different times in the context of sexual selection.
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            How flies get their size: genetics meets physiology.

            Body size affects important fitness variables such as mate selection, predation and tolerance to heat, cold and starvation. It is therefore subject to intense evolutionary selection. Recent genetic and physiological studies in insects are providing predictions as to which gene systems are likely to be targeted in selecting for changes in body size. These studies highlight genes and pathways that also control size in mammals: insects use insulin-like growth factor (IGF) and Target of rapamycin (TOR) kinase signalling to coordinate nutrition with cell growth, and steroid and neuropeptide hormones to terminate feeding after a genetically encoded target weight is achieved. However, we still understand little about how size is actually sensed, or how organ-intrinsic size controls interface with whole-body physiology.
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              Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides.

              The doublesex (dsx) gene regulates somatic sexual differentiation in both sexes in D. melanogaster. Two functional products are encoded by dsx: one product is expressed in females and represses male differentiation, and the other is expressed in males and represses female differentiation. We have determined that the dsx gene is transcribed to produce a common primary transcript that is alternatively spliced and polyadenylated to yield male- and female-specific mRNAs. These sex-specific mRNAs share a common 5' end and three common exons, but possess alternative sex-specific 3' exons, thus encoding polypeptides with a common amino-terminal sequence but sex-specific carboxyl termini. Genetic and molecular data suggest that sequences including and adjacent to the female-specific splice acceptor site play an important role in the regulation of dsx expression by the transformer and transformer-2 loci.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                January 2014
                January 2014
                16 January 2014
                : 10
                : 1
                : e1004098
                Affiliations
                [1 ]Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan
                [2 ]Department of Entomology, Washington State University, Pullman, Washington, United States of America
                [3 ]Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, Japan
                [4 ]Ecological Genetics Laboratory, Center for Frontier Research, National Institute of Genetics, Mishima, Shizuoka, Japan
                [5 ]Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan
                [6 ]Division of Biological Sciences, The University of Montana-Missoula, Missoula, Montana, United States of America
                University of California Davis, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HG HM AI YI TM. Performed the experiments: HG. Analyzed the data: HG HM AI YI LCL DJE TM. Contributed reagents/materials/analysis tools: HG HM AI YI YS. Wrote the paper: HG HM AI YI YS LCL DJE TM.

                Article
                PGENETICS-D-13-01767
                10.1371/journal.pgen.1004098
                3894178
                24453990
                d8a9b454-756a-423b-b054-6d0fd5816225
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 July 2013
                : 26 November 2013
                Page count
                Pages: 9
                Funding
                This work was supported by a Grant-in-Aid for Young Scientists (No. 21677001) from the Ministry of Education, Culture, Sports, Science and Technology of Japan ( https://kaken.nii.ac.jp/d/p/21677001.en.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Developmental Biology
                Evolutionary Biology
                Genetics
                Zoology

                Genetics
                Genetics

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