Molecular Evolution of Sex-Biased Genes in Drosophila

Abstract

Studies of morphology, interspecific hybridization, protein/DNA sequences, and levels of gene expression have suggested that sex-related characters (particularly those involved in male reproduction) evolve rapidly relative to non-sex-related characters. Here we report a general comparison of evolutionary rates of sex-biased genes using data from cDNA microarray experiments and comparative genomic studies of Drosophila. Comparisons of nonsynonymous/synonymous substitution rates (d(N)/d(S)) between species of the D. melanogaster subgroup revealed that genes with male-biased expression had significantly faster rates of evolution than genes with female-biased or unbiased expression. The difference was caused primarily by a higher d(N) in the male-biased genes. The same pattern was observed for comparisons among more distantly related species. In comparisons between D. melanogaster and D. pseudoobscura, genes with highly biased male expression were significantly more divergent than genes with highly biased female expression. In many cases, orthologs of D. melanogaster male-biased genes could not be identified in D. pseudoobscura through a Blast search. In contrast to the male-biased genes, there was no clear evidence for accelerated rates of evolution in female-biased genes, and most comparisons indicated a reduced rate of evolution in female-biased genes relative to unbiased genes. Male-biased genes did not show an increased ratio of nonsynonymous/synonymous polymorphism within D. melanogaster, and comparisons of polymorphism/divergence ratios suggest that the rapid evolution of male-biased genes is caused by positive selection.

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

“…Maleand female-biased genes, especially if sex-biased gene expression has arisen from sexual antagonism, are predicted to have nonrandom genomic distributions depending on the heterogametic system (Rice 1984) or incomplete dosage compensation. This could influence studies of fast-Z as male-biased genes evolve more quickly (Zhang et al 2004;Zhang and Parsch 2005), possibly because of their involvement with sexual selection or malemale competition. If these genes are over-or under-represented on the sex chromosome, this will impact on the mean rates of divergence of sex-linked genes.…”

“…There is evidence that the avian Z chromosome has an excess of coding regions that exhibit a male-biased expression pattern (Kaiser and Ellegren 2006;Storchova and Divinia 2006), which has been shown to be positively correlated with the rate of evolution Zhang et al 2004;Zhang and Parsch 2005). Therefore, we wanted to investigate the relationship between gene expression pattern and d N /d S values in order to determine whether the pattern of fast-Z described above is simply the result of the hyperaccumulation of male-biased genes on the avian Z chromosome.…”

“…) of gene expression data in chicken brain tissue. Any coding region that exhibited twofold or greater bias in males compared to females was designated as male biased, according to previous studies of the relationship between male-biased gene expression and rates of evolution (Zhang et al 2004;Pröschel et al 2005;Zhang and Parsch 2005). We repeated the above described statistical treatments for the data set excluding these identified as coding regions from both the Z and autosomal categories.…”

Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila

“…Within these sex-biased genes, those with male-biased expression tend to show greater difference in expression levels than do female-biased genes or non-sex-biased genes in both within-and between-species comparisons Parisi et al 2003Parisi et al , 2004Ranz et al 2003). In addition, rates of sequence evolution of sex and reproduction-related (SRR) and non-SRR genes differ quite dramatically: male and female SRR genes evolve faster than non-SRR genes (Begun et al 2000;Swanson et al 2001;Zhang et al 2004;Jagadeeshan and Singh 2005;Mueller et al 2005;Proschel et al 2006;Lawniczak and Begun 2007; see Swanson and Vacquier 2002 for review).…”

“…Such studies reported that genes expressed in the testis and genes encoding seminal fluid proteins include many that evolve rapidly (Begun et al 2000Swanson et al 2001;Holloway and Begun 2004;Kern et al 2004;Zhang et al 2004;Begun and Lindfors 2005;Mueller et al 2005;Wagstaff and Begun 2005a;Schully and Hellberg 2006). Many female reproductive proteins have also been shown to evolve faster than non-sexspecific proteins (Civetta and Singh 1995;Jansa et al 2003;Swanson et al 2004;Jagadeeshan and Singh 2005).…”