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Evolution of determinants in sex-determination: A novel hypothesis for the origin of environmental contingencies in avian sex-bias

Journal

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY
Volume 20, Issue 3, Pages 304-312

Publisher

ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD
DOI: 10.1016/j.semcdb.2008.11.013

Keywords

Avian meiosis; Epigenetic effects; Hormones; Segregation distortion; Maternal effects; Adaptive sex-bias

Funding

  1. National Science Foundation [DEB-0075388, IBN-0218313, DEB-0077804]

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Sex-determination is commonly categorized as either genetic or environmental-a classification that obscures the origin of this dichotomy and the evolution of sex-determining factors. The current focus on static outcomes of sex-determination provides little insight into the dynamic developmental processes by which some mechanisms acquire the role of sex determinants. Systems that combine genetic pathways of sex-determination (i.e., sex chromosomes) with environmental pathways (e. g., epigenetically induced segregation distortion) provide an opportunity to examine the evolutionary relationships between the two classes of processes and, ultimately, illuminate the evolution of sex-determining systems. Taxa with sex chromosomes typically undergo an evolutionary reduction in size of one of the sex chromosomes due to suppressed recombination, resulting in pronounced dimorphism of the sex chromosomes, and setting the stage for emergence of epigenetic compensatory mechanisms regulating meiotic segregation of heteromorphic sex chromosomes. Here we propose that these dispersed and redundant regulatory mechanisms enable environmental contingency in genetic sex-determination in birds and account for frequently documented context-dependence in avian sex-determination. We examine the evolution of directionality in such sex-determination as a result of exposure of epigenetic regulators of meiosis to natural selection and identify a central role of hormones in integrating female reproductive homeostasis, resource allocation to oocytes, and offspring sex. This approach clarifies the evolutionary relationship between sex-specific molecular genetic mechanisms of sex-determination and non-sex-specific epigenetic regulators of meiosis and demonstrates that both can determine sex. Our perspective show show non-sex-specific mechanisms can acquire sex-determining function and, by establishing the explicit link between physiological integration of oogenesis and sex-determination, opens new avenues to the studies of adaptive sex-bias and sex-specific resource allocation in species with genetic sex-determination. (C) 2008 Elsevier Ltd. All rights reserved.

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