Widespread Adaptive Evolution of Drosophila Genes with Sex-Biased Expression

By Pröschel, Matthias; Zhang, Zhi et al. | Genetics, October 2006 | Go to article overview

Widespread Adaptive Evolution of Drosophila Genes with Sex-Biased Expression


Pröschel, Matthias, Zhang, Zhi, Parsch, John, Genetics


ABSTRACT

Many genes in higher eukaryotes show sexually dimorphic expression, and these genes tend to be among the most divergent between species. In most cases, however, it is not known whether this rapid divergence is caused by positive selection or if it is due to a relaxation of selective constraint. To distinguish between these two possibilities, we surveyed DNA sequence polymorphism in 91 Drosophila melanogaster genes with male, female-, or nonsex-biased expression and determined their divergence from the sister species D. simulans. Using several single- and multilocus statistical tests, we estimated the type and strength of selection influencing the evolution of the proteins encoded by genes of each expression class. Adaptive evolution, as indicated by a relative excess of nonsynonymous divergence between species, was common among the sex-biased genes (both male and female). Male-biased genes, in particular, showed a strong and consistent signal of positive selection, while female-biased genes showed more variation in the type of selection they experience. Genes expressed equally in the two sexes, in contrast, showed no evidence for adaptive evolution between D. melanogaster and D. simulans. This suggests that sexual selection and intersexual coevolution are the major forces driving genetic differentiation between species.

MALES and females of animal species often differ in many morphological and behavioral traits. This sexual dimorphism has long fascinated biologists and served as the inspiration for Darwin's theory of sexual selection (DARWIN 1871). Recent microarray studies have revealed that sexual dimorphism is also common at the level of gene expression (PARISI et al. 2003; RANZ et al. 2003; GIBSON et al. 2004). For example, ~30% of all genes in Drosophila melanogaster show a twofold or greater difference in expression between the sexes (PARISI et al. 2004). Comparative genomic studies have shown that such sex-biased genes, particularly those with male-biased expression, are among the most rapidly evolving genes between species (SWANSON et al. 2001; ZHANG et al. 2004; KHAITOVICH et al. 2005; RICHARDS et al. 2005). This raises the possibility that adaptive processes, such as sexual selection, may drive the evolution of a large number of genes with sexually dimorphic expression (CIVETTA and SINGH 1999; SINGH and KULATHINAL 2000). An alternate possibility, however, is that sex-biased genes evolve under relaxed selective constraint, which allows them to accumulate more neutral (or nearly neutral) changes between species. For instance, the product of an autosomal gene with sex-specific expression will be visible to selection only over half of its evolutionary history when it is in the appropriate sex. The rest of the time, it will be in the sex where it is not expressed and will be invisible to selection. Thus, it may experience only half as much purifying selection as a gene expressed equally in the two sexes (BARKER et al. 2005).

In some well-studied cases, the rapid evolution of male-biased genes has been attributed to positive selection (SWANSON and VACQUIER 2002). In particular, the male reproductive genes of Drosophila, including those encoding accessory gland proteins (Acp's), appear to be a rich source of adaptively evolving genes (TSAUR and WU 1997; TSAUR et al. 1998; AGUADÉ 1998, 1999; NURMINSKY et al. 1998; TING et al. 1998; BEGUN et al. 2000; BETRÁN and LONG 2003). However, the evolutionary forces affecting the vast majority of male-biased genes are unknown. Although they have been less studied than male-biased genes, there is also evidence for positive selection driving the rapid evolution of particular female-biased genes (SWANSON and VACQUIER 2002). In these cases, either cooperative or antagonistic coevolution between male and female reproductive proteins is thought to play an important role (CIVETTA and SINGH 2005). For example, a survey of expressed sequence tags (ESTs) from the female reproductive tract of D. …

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