The Genetic Basis of Reduced Sexual Dimporphism for Red Throat Color Evolution in the Threespine Stickleback

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DESCRIPTION (provided by applicant): PROJECT SUMMARY Sexual dimorphism pervades all aspects of biology, from evolution to physiology to medicine. Because it contributes to variation in the onset, prevalence, and severity of disease between males and females, sexual dimorphism is in many cases fundamental to understanding and treating complex human diseases. However, a thorough understanding of the genomic basis of variation in sexually dimorphic phenotypes is lacking for almost all organisms, including humans. Studies that integrate genomic and comparative evolutionary approaches to studying sexually dimorphic traits hold potential for rapid progress. Here it is proposed to use an emerging evolutionary and genomic model, the threespine stickleback fish (Gasterosteus aculeatus), to study the genomic basis of variation in sexual dimorphism within a well-characterized evolutionary context. This study will elucidate the genomic underpinnings of male and female ornaments, for carefully chosen natural populations, as a test of the hypothesis that intersexual genetic correlations are mainly responsible for reduced sexual dimorphism. The evolutionary relationships among threespine stickleback populations make this species complex particularly powerful for comparative analyses. Freshwater-resident populations are derived, often in an independent and replicated manner, from the ancestral marine form. In most localities one of the most conspicuously dimorphic stickleback traits is orange-red nuptial coloration on the throats of males but not females. Recently however, the McKinnon laboratory has discovered and begun to study novel populations of stream-resident sticklebacks in which females have evolved the male-typical throat coloration and sexual dimorphism has been reduced. Thus the masculinized female trait has evolved from an ancestral state, in marine populations, in which it is absent but for which extant natural populations are readily sampled. Inter-sexual genetic correlations are expected to have a substantial influence on the evolution of such reduced sexual dimorphism; yet, the genetic basis of variation in sexual dimorphism is almost unknown. Therefore, the primary goal of this proposal is to investigate the genomic basis of variation in sexual dimorphism to answer the question: Does reduced sexual dimorphism result from shared genomic variation between males and females? This work will be accomplished across three specific aims (SA) using state-of-the-art genome wide analyses, quantitative trait loci (QTL) mapping and RNA sequencing (RNA-seq), to study genomic variation associated with variation in sexually dimorphic red throat coloration. Aim 1: Determine whether the same genomic regions contribute to red throat coloration in females and males. Aim 2: Test whether patterns of gene expression are similar between the sexes and convergent populations, and whether colorful females are broadly masculinized, using whole transcriptome analysis. Aim 3: Integrate inferences concerning genetic mechanisms emerging from QTL and gene expression studies.