Sex-biased transcriptome evolution in Drosophila

Genome Biol Evol. 2012;4(11):1189-200. doi: 10.1093/gbe/evs093.

Abstract

Sex-biased genes are thought to drive phenotypic differences between males and females. The recent availability of high-throughput gene expression data for many related species has led to a burst of investigations into the genomic and evolutionary properties of sex-biased genes. In Drosophila, a number of studies have found that X chromosomes are deficient in male-biased genes (demasculinized) and enriched for female-biased genes (feminized) and that male-biased genes evolve faster than female-biased genes. However, studies have yielded vastly different conclusions regarding the numbers of sex-biased genes and forces shaping their evolution. Here, we use RNA-seq data from multiple tissues of Drosophila melanogaster and D. pseudoobscura, a species with a recently evolved X chromosome, to explore the evolution of sex-biased genes in Drosophila. First, we compare several independent metrics for classifying sex-biased genes and find that the overlap of genes identified by different metrics is small, particularly for female-biased genes. Second, we investigate genome-wide expression patterns and uncover evidence of demasculinization and feminization of both ancestral and new X chromosomes, demonstrating that gene content on sex chromosomes evolves rapidly. Third, we examine the evolutionary rates of sex-biased genes and show that male-biased genes evolve much faster than female-biased genes, which evolve at similar rates to unbiased genes. Analysis of gene expression among tissues reveals that this trend may be partially due to pleiotropic effects of female-biased genes, which limits their evolutionary potential. Thus, our findings illustrate the importance of accurately identifying sex-biased genes and provide insight into their evolutionary dynamics in Drosophila.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Chromosome Mapping
  • Cluster Analysis
  • Drosophila / genetics*
  • Drosophila melanogaster / genetics
  • Evolution, Molecular*
  • Female
  • Gene Expression
  • Genes, Insect
  • Genes, X-Linked
  • Male
  • Sex Characteristics*
  • Transcriptome / genetics*
  • X Chromosome / genetics