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      Sex-Specific Weight Loss Mediates Sexual Size Dimorphism in Drosophila melanogaster

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      PLoS ONE
      Public Library of Science

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          Abstract

          The selective pressures leading to the evolution of Sexual Size Dimorphism (SSD) have been well studied in many organisms, yet, the underlying developmental mechanisms are poorly understood. By generating a complete growth profile by sex in Drosophila melanogaster, we describe the sex-specific pattern of growth responsible for SSD. Growth rate and critical size for pupariation significantly contributed to adult SSD, whereas duration of growth did not. Surprisingly, SSD at peak larval mass was twice that of the uneclosed adult SSD with weight loss between peak larval mass and pupariation playing an important role in generating the final SSD. Our finding that weight loss is an important regulator of SSD adds additional complexity to our understanding of how body size is regulated in different sexes. Collectively, these data allow for the elucidation of the molecular-genetic mechanisms that generate SSD, an important component of understanding how SSD evolves.

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          Most cited references13

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          A single IGF1 allele is a major determinant of small size in dogs.

          The domestic dog exhibits greater diversity in body size than any other terrestrial vertebrate. We used a strategy that exploits the breed structure of dogs to investigate the genetic basis of size. First, through a genome-wide scan, we identified a major quantitative trait locus (QTL) on chromosome 15 influencing size variation within a single breed. Second, we examined genetic variation in the 15-megabase interval surrounding the QTL in small and giant breeds and found marked evidence for a selective sweep spanning a single gene (IGF1), encoding insulin-like growth factor 1. A single IGF1 single-nucleotide polymorphism haplotype is common to all small breeds and nearly absent from giant breeds, suggesting that the same causal sequence variant is a major contributor to body size in all small dogs.
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            Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4.

            The control of growth is fundamental to the developing metazoan. Here, we show that CHICO, a Drosophila homolog of vertebrate IRS1-4, plays an essential role in the control of cell size and growth. Animals mutant for chico are less than half the size of wild-type flies, owing to fewer and smaller cells. In mosaic animals, chico homozygous cells grow slower than their heterozygous siblings, show an autonomous reduction in cell size, and form organs of reduced size. Although chico flies are smaller, they show an almost 2-fold increase in lipid levels. The similarities of the growth defects caused by mutations in chico and the insulin receptor gene in Drosophila and by perturbations of the insulin/IGF1 signaling pathway in vertebrates suggest that this pathway plays a conserved role in the regulation of overall growth by controling cell size, cell number, and metabolism.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                28 March 2013
                : 8
                : 3
                : e58936
                Affiliations
                [1]Department of Zoology and Ecology and Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan, United States of America
                MRC, University College of London, United Kingdom
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NDT SMG AWS. Performed the experiments: NDT SMG. Analyzed the data: NDT AWS. Contributed reagents/materials/analysis tools: AWS. Wrote the paper: NDT AWS.

                Article
                PONE-D-12-37912
                10.1371/journal.pone.0058936
                3610704
                23555608
                6b5ebbc2-2624-40cd-a3be-b8ed09d92411
                Copyright @ 2013

                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
                : 30 November 2012
                : 8 February 2013
                Page count
                Pages: 5
                Funding
                This research was supported by National Science Foundation grants IOS-0919855 and IOS-0845847 to AWS, and fellowship support from Michigan State University to NDT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Physiological Processes
                Developmental Biology
                Morphogenesis
                Growth Control
                Sexual Differentiation
                Organism Development
                Model Organisms
                Animal Models
                Drosophila Melanogaster

                Uncategorized
                Uncategorized

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