A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: Evidence for masculinization of the transcriptome

Abstract

BackgroundIn many taxa, males and females are very distinct phenotypically, and these differences often reflect divergent selective pressures acting on the sexes. Phenotypic sexual dimorphism almost certainly reflects differing patterns of gene expression between the sexes, and microarray studies have documented widespread sexually dimorphic gene expression. Although the evolutionary significance of sexual dimorphism in gene expression remains unresolved, these studies have led to the formulation of a hypothesis that male-driven evolution has resulted in the masculinization of animal transcriptomes. Here we use a microarray assessment of sex- and gonad-biased gene expression to test this hypothesis in zebrafish.ResultsBy using zebrafish Affymetrix microarrays to compare gene expression patterns in male and female somatic and gonadal tissues, we identified a large number of genes (5899) demonstrating differences in transcript abundance between male and female Danio rerio. Under conservative statistical significance criteria, all sex-biases in gene expression were due to differences between testes and ovaries. Male-enriched genes were more abundant than female-enriched genes, and expression bias for male-enriched genes was greater in magnitude than that for female-enriched genes. We also identified a large number of genes demonstrating elevated transcript abundance in testes and ovaries relative to male body and female body, respectively.ConclusionOverall our results support the hypothesis that male-biased evolutionary pressures have resulted in male-biased patterns of gene expression. Interestingly, our results seem to be at odds with a handful of other microarray-based studies of sex-specific gene expression patterns in zebrafish. However, ours was the only study designed to address this specific hypothesis, and major methodological differences among studies could explain the discrepancies. Regardless, all of these studies agree that transcriptomic sex differences in D. rerio are widespread despite the apparent absence of heterogamety. These differences likely make important contributions to phenotypic sexual dimorphism in adult zebrafish; thus, from an evolutionary standpoint, the precise roles of sex-specific selection and sexual conflict in the evolution of sexually dimorphic gene expression are very important. The results of our study and others like it set the stage for further work aimed at directly addressing this exciting issue in comparative genomics.

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

“…These differences were not due to temperature but to sex, and represent a substantial proportion of protein-coding genes in zebrafish (43). This concurs with previous observations (44)(45)(46) showing large sex-related differences in the gonadal transcriptome of the adult zebrafish.…”

Comparative expression analysis in mature gonads, liver and brain of turbot (Scophthalmus maximus) by cDNA-AFLPS

“…Some microarray-based studies on sex-specific gene expression patterns showed an important masculinization of the transcriptome (Small, et al, 2009). In Drosophila melanogaster recent works have shown that sex-biased gene expression is significant in Drosophila, especially in gonads.…”

“…Most of these studies have been focused in a few genes, being Dmrt1 the most analyzed because it is the only known non-mammalian vertebrate master sex-determining gene (Matsuda et al, 2002;Nanda et al, 2002). Large-scale gene expression studies have been made in a few fish species including zebrafish (Small et al, 2009), medaka (Lo et al, 2008), perch (Rossi et al, 2007), sea bass (Chini et al, 2006;Kulh et al, 2010), blue fin tuna (Chini et al, 2008) and three spine sticklebacks (Leder et al, 2010).…”

Sex-Biased Gene Expression and Sexual Conflict throughout Development: Table 1.

“…For example, in mice, patterns of sex-biased gene expression vary between different tissues (Rinn et al 2004;Yang et al 2006). In zebrafish, Danio rerio, sex bias in the transcriptome of the brain tissue was found to be quite low ( 2%) (Santos et al 2008), but a different study identified sex biases across 38% of the transcriptome that were attributed to differences in gene expression in male and female reproductive tissues (Small et al 2009). Similarly, in the silkworm Bombyx mori, sex-biased gene expression varied between 2% and 30%, depending on the tissue examined (Xia et al 2007).…”