The Evolution of Sex-Related Traits and Genes

Abstract

A growing number of studies are drawing attention to a consistent pattern of rapid evolution of sex-related traits and genes. Different hypotheses have been proposed to explain this rapid divergence. For traits and genes directly involved in reproduction, the pressures imposed by different sexes are likely to have driven rapid evolution, either by conflictive interactions, forms of female cryptic choice (female sex drive), or male differential use of traits and behavioral tactics (male sex drive). However, other factors such as subfunc-tionalization linked to gene duplications, birth and death processes, and pleiotropic effects, particularly those linked to immunity, can also drive fast change. The disruption of reproductive traits and gene interactions are of interest to those studying speciation because they can impede gene flow among diverging populations. Different studies have also shown that rapid changes and adaptive diversification between species can occur in reproductive developmental processes such as sex determination and gamete formation. Finally, high-throughput molecular technologies and bioin-formatics approaches are allowing us to place patterns of gene evolution within the broad context of whole genome dynamics. The ten papers published in this Issue tackle some of these fundamental questions on the evolution of sex-related traits and genes. Three opening review articles address problems relating to testing sexual selection at the molecular level, gene duplications and the evolution of sex bias patterns of gene expression, and the evolutionary origin of game-togenesis. A. Wong reviews recent studies in rodents and primates that have tested for associations between proxies of sexual selection and rates of evolution on male reproductive genes. He highlights how only a few studies have been able to establish significant associations. While this might cast some doubts on the role of sexual selection on the rapid evolution of male reproductive genes, he brings up some of the analytical problems linked to these prior studies and the need to incorporate multigene analysis and population genetics-based approaches. In their review, M. Gallach and collaborators address the problem faced by sexually reproducing species due to the need to generate two sexes with different patterns of tissue-specific gene expression and physiologies. They show that this conflict between sexes has led to a nonrandom distribution of sex-biased genes in different species and that gene duplication can help avoid sex-related genomic clashes leading to dosage compensation or meiotic sex chromosome inactivation as well as alleviate sexual conflict within species. Lastly, J. M. Eirín-L ´ opez and J. Ausí o provide an up-to-date insight into the evolutionary origins of the molecular mechanisms underlying sexual reproduction in metazoan animals. By bringing attention into the recent characterization of the DAZ family of reproductive proteins, the authors suggest that the wide conservation of a core reproductive machinery encoded by premeiotically expressed genes across Metazoa lends support to a common evolutionary origin for gametogenesis, rejecting the hypothesis that gametogenesis evolved multiple times in different lineages. Seven research articles also address a variety of questions related to the evolution of sex-related traits and genes. Fox et al. reanalyzed data from seven human populations to show preferential paternal grandmothering behavior towards