Sexually antagonistic selection (or SAS) acts when an allele is beneficial to one sex but deleterious to the other. It is thought to be important to the maintenance of genetic diseases, variation in social behaviors, and evolution of genome structure. Despite its importance to evolution, we know little about the genomic impact of SAS in natural populations because the classical tools of molecular evolution cannot detect it. This project will advance our understanding of SAS in two dimensions:
Aim 1 will use new methods to detect SAS by measuring the small differences between allele frequencies in males and females that result from SAS acting in the current generation. Individually, these differences are rarely statistically significant, but we recently discovered that these differences can be aggregated across the genome to detect and quantify SAS. We will apply this strategy to large samples of whole genomes from natural populations of stickleback fishes that differ in their degree of sexual dimorphism. The results will provide the first estimates of the genome-wide strength of SAS, and the total amount of mortality imposed on males and females because individuals carry alleles that are adapted to the other sex.
Aim 2 will provide the first systematic test of the prevailing hypothesis that SAS drives transitions between XY and ZW sex chromosome systems. These transitions are key events in genome evolution: they rewire the sex determination pathway, can trigger the degeneration of the Y or W chromosome, and have downstream effects on population demography. While theory shows these transitions can result from SAS, no systematic test of the hypothesis has been carried out. The research will focus on poeciliid fishes that vary both within and between species for XY and ZW sex determination. A novel strategy will be used to obtain the phased sequences of X, Y, Z, and W chromosomes. Gene trees for these chromosomes will show the sequence in which they evolved, test a key prediction of the SAS hypothesis, and give unprecedented views of very young W sex chromosomes. The research will have two major kinds of broader impacts. (i) It will develop a new approach for detecting selection acting contemporaneously, and determining its demographic impact. The strategy is a major departure from current methods, which rely on genetic signatures that only accumulate over many generations. The new methods will have applications to diverse forms of selection and to other species, including humans. (ii) The project will develop poeciliid fishes as the first model system in which all four types of sex chromosomes (X, Y, Z, and W) can be studied. Important new research horizons will be opened, for example revealing how confining a sex chromosome to females (the W) alters the mode and tempo of its evolution.

Public Health Relevance

Sexually antagonistic selection is important to the maintenance of genetic diseases, variation in social behaviors, and evolution of genome structure. This project will use a new strategy to obtain the first measurements of sexually antagonistic selection and its impacts on the viability of females and males in natural populations of fishes. It will then provide the first test of the prevailing hypothesis that sexually antagonistic selection is responsible for one of the most dramatic events that can occur to a eukaryotic genome: a transition between sex determination by XY and ZW chromosomes.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Genetic Variation and Evolution Study Section (GVE)
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Janes, Daniel E
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University of Texas Austin
Schools of Arts and Sciences
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Dixon, Groves; Kitano, Jun; Kirkpatrick, Mark (2018) The origin of a new sex chromosome by introgression between two stickleback fishes. Mol Biol Evol :
Cheng, Changde; Kirkpatrick, Mark (2018) Inversions are bigger on the X chromosome. Mol Ecol :
Pennell, Matthew W; Mank, Judith E; Peichel, Catherine L (2018) Transitions in sex determination and sex chromosomes across vertebrate species. Mol Ecol 27:3950-3963
Sardell, Jason M; Cheng, Changde; Dagilis, Andrius J et al. (2018) Sex Differences in Recombination in Sticklebacks. G3 (Bethesda) 8:1971-1983
Cheng, Changde; Kirkpatrick, Mark (2017) Environmental Plasticity in the Intersexual Correlation and Sex Bias of Gene Expression. J Hered 108:754-758
Fontaine, Albin; Filipovic, Igor; Fansiri, Thanyalak et al. (2017) Extensive Genetic Differentiation between Homomorphic Sex Chromosomes in the Mosquito Vector, Aedes aegypti. Genome Biol Evol 9:2322-2335
Kirkpatrick, Mark (2017) The Evolution of Genome Structure by Natural and Sexual Selection. J Hered 108:3-11
Peichel, Catherine L (2017) Chromosome Evolution: Molecular Mechanisms and Evolutionary Consequences. J Hered 108:1-2
Peichel, Catherine L; Marques, David A (2017) The genetic and molecular architecture of phenotypic diversity in sticklebacks. Philos Trans R Soc Lond B Biol Sci 372:
Peichel, Catherine L; Sullivan, Shawn T; Liachko, Ivan et al. (2017) Improvement of the Threespine Stickleback Genome Using a Hi-C-Based Proximity-Guided Assembly. J Hered 108:693-700

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