Differences between males and females in the optimal phenotype that is favoured by selection can be resolved by the evolution of differential gene expression in the two sexes. Microarray experiments have shown that such sex-biased gene expression is widespread across organisms and genomes. Sex-biased genes show unusually rapid sequence evolution, are often labile in their pattern of expression, and are non-randomly distributed in the genome. Here we discuss the characteristics and expression of sex-biased genes, and the selective forces that shape this previously unappreciated source of phenotypic diversity. Sex-biased gene expression has implications beyond just evolutionary biology, including for medical genetics.
Females and males often differ extensively in their physical traits. This sexual dimorphism is largely caused by differences in gene expression. Recent advances in genomics, such as RNA sequencing (RNA-seq), have revealed the nature and extent of sex-biased gene expression in diverse species. Here we highlight new findings regarding the causes of sex-biased expression, including sexual antagonism and incomplete dosage compensation. We also discuss how sex-biased expression can accelerate the evolution of sex-linked genes.
A number of genes associated with sexual traits and reproduction evolve at the sequence level faster than the majority of genes coding for non-sex-related traits. Whole genome analyses allow this observation to be extended beyond the limited set of genes that have been studied thus far. We use cDNA microarrays to demonstrate that this pattern holds in Drosophila for the phenotype of gene expression as well, but in one sex only. Genes that are male-biased in their expression show more variation in relative expression levels between conspecific populations and two closely related species than do female-biased genes or genes with sexually monomorphic expression patterns. Additionally, elevated ratios of interspecific expression divergence to intraspecific expression variation among male-biased genes suggest that differences in rates of evolution may be due in part to natural selection. This finding has implications for our understanding of the importance of sexual dimorphism for speciation and rates of phenotypic evolution.A nisogamous reproduction is common in many animal and plant species and can produce a number of conflicts with important evolutionary consequences. For example, differential selection coefficients between the two sexes can lead to stable genetic polymorphisms or a decline in population mean fitness (1). It can also drive accelerated rates of phenotypic evolution, as many morphologies associated with sex and reproduction diverge more rapidly than other phenotypes (2). Molecular techniques that provide rapid and quantitative measures of genotypic and phenotypic variation have extended this pattern to include accelerated rates of evolution among proteins with sexual or reproductive functions (3, 4). Since then, most data supporting this observation have come from homologous nucleotide sequences of genes that are associated with sex or reproduction. In ciliates, green algae, diatoms, angiosperms, fungi, and at least four animal phyla, unusually high ratios of nonsynonymous to synonymous substitutions (d N ͞d S ) between species have been documented in sex-related genes (reviewed in ref. 5). Some of these genes also show high levels of intraspecific differentiation (5). In Drosophila, much of this work has focused on genes that are expressed in testes or accessory glands (e.g., refs. 6 and 7), although a high d N ͞d S has also been observed for genes expressed in females and components of the sex determination pathway (8).Protein coding sequences provide a natural context for studying rates of evolution, as the effect of a given nucleotide substitution on the polypeptide is predictable, and comparison between neighboring synonymous and nonsynonymous sites controls for mutation rate. Because of the lack of an analogous context for regulatory sequences, the rates and patterns of evolution in regions of the genome controlling gene expression are less well understood. Thus, it is not known whether the rapid rates of evolution among genes associated with sex and reproduction holds for gene expression as w...
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