Fast evolutionary turnover and overlapping variances of sex-biased gene expression patterns defy a simple binary sex classification of somatic tissues.

Abstract

Sexual dimorphism in phenotypes is largely driven by genes with sex-biased expression, spanning from key regulators to numerous organ-specific effectors. Current understanding is limited regarding the evolutionary dynamics of these genes in somatic tissues that generate the adult phenotype versus gonadal organs that are required for reproduction. Here, we investigate sex-biased gene expression and micro-evolutionary patterns of these genes in populations of subspecies and species of wild mice (genus Mus) that were raised under controlled conditions. We find a faster evolutionary turnover of sex-biased gene expression in somatic tissues, but not in the gonads, when compared to the turnover of non-sex-biased genes. We introduce a sex-biased gene expression index (SBI) to quantify individual variances. We find a range from binary to overlapping SBI patterns across individuals. SBI values do not correlate between organs of the same individuals, thus supporting a mosaic model of somatic sex determination. Comparison with data from humans shows mostly fewer sex-biased genes compared to mice and strongly overlapping SBI distributions between the somatic organs of the sexes. We conclude that adult individuals are composed of a mosaic spectrum of sex characteristics in their somatic tissues that should not be cumulated into a simple binary classification.