TY - JOUR
T1 - Evolution of "determinants" in sex-determination
T2 - A novel hypothesis for the origin of environmental contingencies in avian sex-bias
AU - Uller, Tobias
AU - Badyaev, Alexander V.
N1 - Funding Information:
We are grateful to David Crews for the invitation to contribute and helpful suggestions and to Renee Duckworth, Philip Bergmann, Caroline Isaksson, Kevin Oh, and Libby Landeen for insightful discussion and comments on this manuscript. This work was supported by a Fulbright Foundation Fellowship to TU and the David and Lucille Packard Fellowship to AVB. Empirical work on sex-determination in the house finch was funded by the grants from the National Science Foundation (DEB-0075388, IBN-0218313, and DEB-0077804).
PY - 2009/5
Y1 - 2009/5
N2 - 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 shows how 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.
AB - 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 shows how 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.
KW - Adaptive sex-bias
KW - Avian meiosis
KW - Epigenetic effects
KW - Hormones
KW - Maternal effects
KW - Segregation distortion
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U2 - 10.1016/j.semcdb.2008.11.013
DO - 10.1016/j.semcdb.2008.11.013
M3 - Review article
C2 - 19073270
AN - SCOPUS:63849083596
VL - 20
SP - 304
EP - 312
JO - Seminars in Cell and Developmental Biology
JF - Seminars in Cell and Developmental Biology
SN - 1084-9521
IS - 3
ER -