Rapid Evolution of Female-Biased, but Not Male-Biased, Genes Expressed in the Avian Brain

Abstract

The powerful pressures of sexual and natural selection associated with species recognition and reproduction are thought to manifest in a faster rate of evolution in sex-biased genes, an effect that has been documented particularly for male-biased genes expressed in the reproductive tract. However, little is known about the rate of evolution for genes involved in sexually dimorphic behaviors, which often form the neurological basis of intrasexual competition and mate choice. We used microarray data, designed to uncover sex-biased expression patterns in embryonic chicken brain, in conjunction with data on the rate of sequence evolution for >4,000 coding regions aligned between chicken and zebra finch in order to study the role of selection in governing the molecular evolution for sex-biased and unbiased genes. Surprisingly, we found that female-biased genes, defined across a range of cutoff values, show a higher rate of functional evolution than both male-biased and unbiased genes. Autosomal male-biased genes evolve at a similar rate as unbiased genes. Sex-specific genomic properties, such as heterogeneity in genomic distribution and GC content, and codon usage bias for sex-biased classes fail to explain this surprising result, suggesting that selective pressures may be acting differently on the male and female brain.

Polyandry and sex-specific gene expression

“…However, the opposite has been observed, as whole-body and aggregate transcriptome studies actually underestimate the degree of sex-bias within constituent parts [40,85,86]. This is particularly problematic for studies of brain transcription: although fine scale analysis of gene expression in the brain has revealed profound sex-bias in limited areas that control sex-specific behaviours [130], whole-brain or partial-brain homogenates reveal very little overall sex-bias [39,40] because sex-specific expression of different genes in different regions is averaged, and localized differences are therefore diluted. This suggests that the initial estimates of whole-body sexbias in roughly half of all genes are in fact underestimates, rather than overestimates, and that finer-scale dissections will reveal more pervasive patterns of local sex-biased gene expression.…”

Are sex-biased genes more dispensable?

“…Sex-biased loci in general exhibit an accelerated rate of protein evolution, and many authors (including ourselves) have posited that this results from the powerful pressures of sexual selection (Zhang et al 2004;Prö schel et al 2006;Ellegren & Parsch 2007;Mank et al 2007). Clearly, positive selection is a driver in the evolution of male reproductive proteins associated with sperm competition and fertilization (Zhang et al 2004;Begun & Lindfors 2005); however, sexual selection has been invoked to explain the accelerated rates of evolution for broader categories of sex-biased genes as well (Zhang et al 2004;Prö schel et al 2006).…”

Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

“…1 Drosophila male-biased genes have higher birth and extinction rates than female-biased or non-sex-biased genes ). However, in birds genes with female-biased expression in the brain show faster rates of sequence evolution than male-biased and non-sexbiased genes (Mank et al 2007). Fourth, male-biased genes also show the highest levels of interspecific gene expression divergence in Drosophila and mammals Ranz et al 2003;Khaitovich et al 2005;Voolstra et al 2007).…”