SMBE 2014: Insights on Sexually Antagonistic Selection in the Human Genome

Insights on Sexually Antagonistic Selection in the Human Genome
Elise Lucotte 1, Romain Laurent1 ,2, Laure Segurel1, Evelyne Heyer1, Bruno Toupance1
1Eco-anthropologie et Ethnobiologie, UMR 7206 CNRS, MNHN, Univ Paris Diderot, Sorbonne Paris Cité, F-75005, Paris, France, 2Max Planck Institute for Evolutionary Anthropology, Department of Evolutionary Genetics, Leipzig, Germany
In species with two separate sexes, sexually antagonistic (SA) selection occurs if both sexes undergo selection in opposite direction for a trait. If this trait is coded by the same set of genes in both sexes, an intralocus sexual conflict (IASC) arises. These conflicts initiate the evolution of sexual dimorphism, and can be resolved through sex-biased gene expression. A classical theoretical model proposes that unresolved conflicts may persist in the genome and create stable polymorphisms between the sexes at the population level. This model furthermore predicts that the X chromosome should provide a favorable environment for the accumulation of loci under IASC as compared to the autosomes. Although numerous studies have been conducted to test this hypothesis, they provided conflicting results and, so far, no study attempted to map loci under IASC at the genome-wide level. Here, we propose a new methodological framework designed to detect loci under IASC using high-density genetic data. Using this method on HapMap III, a human genome-wide SNP dataset, we identify SNPs showing significant differences in allelic frequencies between the sexes, a signature expected to be observed at loci undergoing IASC. Our results show that the X chromosome contains more signal of IASC than any other chromosome. Moreover, we find that genes showing a signature of IASC are preferentially involved in the determination of traits known to be sexually dimorphic in humans, including external appearance, metabolism and immune system. We also detect genes involved in developmental processes and regulation of gene expression, which is consistent with an ongoing process of IASCs resolution. Furthermore, we find an extreme signal of differentiation between the sexes in a region containing a chromatin insulator binding site, a structure that mediates long-range genomic interactions and therefore affects epigenetic status and gene expression. Our results demonstrate the existence of unresolved IASCs in humans, and suggest their implication in the evolution of human sexual dimorphisms.

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