Masculinization of Gene Expression Is Associated with Exaggeration of Male Sexual Dimorphism

Abstract

Gene expression differences between the sexes account for the majority of sexually dimorphic phenotypes, and the study of sex-biased gene expression is important for understanding the genetic basis of complex sexual dimorphisms. However, it has been difficult to test the nature of this relationship due to the fact that sexual dimorphism has traditionally been conceptualized as a dichotomy between males and females, rather than an axis with individuals distributed at intermediate points. The wild turkey (Meleagris gallopavo) exhibits just this sort of continuum, with dominant and subordinate males forming a gradient in male secondary sexual characteristics. This makes it possible for the first time to test the correlation between sex-biased gene expression and sexually dimorphic phenotypes, a relationship crucial to molecular studies of sexual selection and sexual conflict. Here, we show that subordinate male transcriptomes show striking multiple concordances with their relative phenotypic sexual dimorphism. Subordinate males were clearly male rather than intersex, and when compared to dominant males, their transcriptomes were simultaneously demasculinized for male-biased genes and feminized for female-biased genes across the majority of the transcriptome. These results provide the first evidence linking sexually dimorphic transcription and sexually dimorphic phenotypes. More importantly, they indicate that evolutionary changes in sexual dimorphism can be achieved by varying the magnitude of sex-bias in expression across a large proportion of the coding content of a genome.

Evolution of opsin expression in birds driven by sexual selection and habitat

“…In birds, differential gene expression has also been associated with sexual differentiation [57]. Here, I found large differences in opsin expression among New World warbler species as well as between the sexes, which can be related to both measures of sexual selection and the light environment.…”

Sexual selection drives evolution and rapid turnover of male gene expression

“…The sizable proportion of genes exhibiting sex-biased expression suggests that sexual selection has the potential to shape many aspects of genome biology. Recent studies of intrasexual variation in gene expression differences between males and females of the same species have revealed patterns of overall transcription consistent with the degree of phenotypic sexual dimorphism (9,10), and experimental manipulation of sex-specific selection affects sex-biased gene expression over short time scales (11)(12)(13). These studies together suggest that increasing sexual selection across species should lead to increased turnover in sex-biased gene expression and a greater sexualization of the transcriptome over longer evolutionary timescales.…”

Sex differences in DNA methylation and expression in zebrafish brain: a test of an extended ‘male sex drive’ hypothesis

“…Not surprisingly, female and male gonads usually differ remarkably in the sets of highly expressed genes [4][5][6][7]. Sex-biased gene expression, although less pronounced than in the gonads, has been also found in many somatic tissues, such as liver, spleen, muscles and brain [4,8,9]. Brain is the second most sexually dimorphic organ after gonads.…”