Rapid evolution of male-biased gene expression in Drosophila

Abstract

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...

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…While there is evidence for rapid evolution of suppressed recombination in D. melanogaster [71][72][73], comparisons of gene regulation between natural D. melanogaster strains indicate that sexbiased expression can also evolve very rapidly [74]. Furthermore, transitions from bisexual to sex-limited expression need not involve complex adaptations.…”

Regulatory evolution across the protein interaction network

“…Recent studies on variation in gene expression in natural populations indicate that a number of factors influence regulatory evolution, including membership in a particular functional class or biological process 1 and the pattern of sex-biased expression 2,3 . Protein-protein interactions may also be relevant to regulatory evolution if they mean that the interacting partners of a given protein impose stricter stoichiometric requirements.…”

“…We analyzed variation in expression of 5,978 yeast (Saccharomyces cerevisiae) genes among four natural isolates grown under identical laboratory conditions 4 , of 4,439 fly (Drosophila melanogaster) genes in adult males from eight wild-type strains of geographically diverse origin 2 and of a similar number of genes assayed in both sexes of two species of Drosophila 3 . We matched these data to protein-protein interactions that could be assigned with high confidence (confidence score 4 0.55): 8,728 in yeast 5 and 3,964 in flies 6 .…”

Gene expression: Fast males

“…Evolutionary biologists are now using microarrays to study global sexbiased gene expression, which until recently has been beyond experimental reach. An excellent example of this is a recent paper by Meiklejohn et al (2003), which explores sex-differential gene expression in Drosophila melanogaster and reports that genes with male-biased expression are more variably expressed between strains. These data strongly support the idea that genes with male functions evolve more rapidly than those used for other functions.…”

“…Microarray analysis shows that roughly 50% of the genes in D. melanogaster show significant sex-biased expression in adults (Jin et al, 2001;Meiklejohn et al, 2003;Ranz et al, 2003), mostly due to differences in the germline (Andrews et al, 2000;Arbeitman et al, 2002;Parisi et al, 2003). Genes with male-biased expression turn over rapidly in terms of both gene expression over a B2.5 million year time scale (compared to D. simulans, Meiklejohn et al, 2003;Ranz et al, 2003) and sequence over a B250 million year time scale (compared to Anopheles gambiae, Parisi et al, 2003).…”