Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle

Genome Biol Evol. 2010 Jul 12:2:336-46. doi: 10.1093/gbe/evq024.

Abstract

A genome's ability to produce two separate sexually dimorphic phenotypes is an intriguing biological mystery. Microarray-based studies of a handful of model systems suggest that much of the mystery can be explained by sex-biased gene expression evolved in response to sexually antagonistic selection. We present the first whole-genome study of sex-biased expression in the red flour beetle, Tribolium castaneum. Tribolium is a model for the largest eukaryotic order, Coleoptera, and we show that in whole-body adults, approximately 20% of the transcriptome is differentially regulated between the sexes. Among T. castaneum, Drosophila melanogaster, and Anopheles gambiae, we identify 416 1:1:1 orthologs with conserved sex-biased expression. Overrepresented functional categories among sex-biased genes are primarily those involved in gamete production and development. The genomic distribution of sex-biased genes in T. castaneum is distinctly nonrandom, with the strongest deficit of male-biased genes on the X chromosome (9 of 793) of any species studied to date. Tribolium also shows a significant enrichment of X-linked female-biased genes (408 of 793). Our analyses suggest that the extensive female bias of Tribolium X chromosome gene expression is due to hyperexpression of X-linked genes in both males and females. We propose that the overexpression of X chromosomes in females is an evolutionary side effect of the need to dosage compensate in males and that mechanisms to reduce female X chromosome gene expression to autosomal levels are sufficient but imperfect.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anopheles / genetics
  • Dosage Compensation, Genetic
  • Drosophila melanogaster / genetics
  • Evolution, Molecular
  • Female
  • Gene Expression
  • Gene Expression Profiling
  • Genes, Insect*
  • Genes, X-Linked*
  • Male
  • Models, Genetic
  • Sex Characteristics
  • Species Specificity
  • Tribolium / genetics*
  • X Chromosome / genetics*