Two Forms of Sexual Dimorphism in Gene Expression in Drosophila melanogaster: Their Coincidence and Evolutionary Genetics.

Phenotypic sexual dimorphism can be mediated by sex differences in gene expression. We examine two forms of sexual dimorphism in gene expression in Drosophila melanogaster: 1) sex-biased gene expression (SBGE) in which the sexes differ in the amount a gene is expressed and 2) sexual dimorphism in isoform usage, that is, sex-specific splicing (SSS). In whole body (but not the head) expression, we find a negative association between SBGE and SSS, possibly suggesting that these are alternate routes to resolving sexual antagonistic selection. Next, we evaluate whether expression dimorphism contributes to the heterogeneity among genes in rmf, the intersexual genetic correlation in body expression that constrains the extent to which a gene's expression can evolve independently between the sexes. We find lower rmf values for genes with than without SSS. We find higher rmf values for male- than female-biased genes (except genes with extreme male bias), even though male-biased genes are known to have greater evolutionary divergence in expression. Finally, we examine population genetic patterns in relation to SBGE and SSS because genes with expression dimorphism have likely experienced a history of sex differences in selection. SSS is associated with reduced values of Tajima's D and elevated direction of selection (DoS) values, suggestive of higher rates of adaptive evolution. Though DoS is highly elevated for genes with extreme male bias, DoS otherwise tends to decline from female-biased to unbiased to male-biased genes. Collectively, the results indicate that SBGE and SSS are differentially distributed across the genome and are associated with different forms of selection.

Singh A ，Agrawal AF 《-》

The shared genome is a pervasive constraint on the evolution of sex-biased gene expression.

Griffin RM ，Dean R ，Grace JL ，Rydén P ，Friberg U ... -  《-》

The evolution of sexual dimorphism in gene expression in response to a manipulation of mate competition.

Many genes are differentially expressed between males and females and patterns of sex-biased gene expression (SBGE) vary among species. Some of this variation is thought to have evolved in response to differences in mate competition among species that cause varying patterns of sex-specific selection. We used experimental evolution to test this by quantifying SBGE and sex-specific splicing in 15 Drosophila melanogaster populations that evolved for 104 generations in mating treatments that removed mate competition via enforced monogamy, or allowed mate competition in either small, simple, or larger, structurally more complex mating environments. Consistent with sex-specific selection affecting SBGE, initially sex-biased genes diverged in expression more among treatments than unbiased genes, and there was greater expression divergence for male- than female-biased genes. It has been suggested the transcriptome should be "feminized" under monogamy because of the removal of sexual selection on males; we did not observe this, likely because selection differs in additional ways between monogamy vs. polygamy. Significant divergence in average expression dimorphism between treatments was observed and, in some treatment comparisons, the direction of the divergence differed across different sex-bias categories. There was not a generalized reduction in expression dimorphism under enforced monogamy.

Mishra P ，Rundle HD ，Agrawal AF 《-》

Gene duplication in the evolution of sexual dimorphism.

Males and females share most of the same genes, so selection in one sex will typically produce a correlated response in the other sex. Yet, the sexes have evolved to differ in a multitude of behavioral, morphological, and physiological traits. How did this sexual dimorphism evolve despite the presence of a common underlying genome? We investigated the potential role of gene duplication in the evolution of sexual dimorphism. Because duplication events provide extra genetic material, the sexes each might use this redundancy to facilitate sex-specific gene expression, permitting the evolution of dimorphism. We investigated this hypothesis at the genome-wide level in Drosophila melanogaster, using the presence of sex-biased expression as a proxy for the sex-specific specialization of gene function. We expected that if sexually antagonistic selection is a potent force acting upon individual genes, duplication will result in paralog families whose members differ in sex-biased expression. Gene members of the same duplicate family can have different expression patterns in males versus females. In particular, duplicate pairs containing a male-biased gene are found more frequently than expected, in agreement with previous studies. Furthermore, when the singleton ortholog is unbiased, duplication appears to allow one of the paralog copies to acquire male-biased expression. Conversely, female-biased expression is not common among duplicates; fewer duplicate genes are expressed in the female-soma and ovaries than in the male-soma and testes. Expression divergence exists more in older than in younger duplicates pairs, but expression divergence does not correlate with protein sequence divergence. Finally, genomic proximity may have an effect on whether paralogs differ in sex-biased expression. We conclude that the data are consistent with a role of gene duplication in fostering male-biased, but not female-biased, gene expression, thereby aiding the evolution of sexual dimorphism.

Wyman MJ ，Cutter AD ，Rowe L 《-》

The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster.

Perry JC ，Harrison PW ，Mank JE 《-》