Parallel faster-X evolution of gene expression and protein sequences in Drosophila: beyond differences in expression properties and protein interactions.

Ana Llopart,Nadia Singh

doi:10.1371/journal.pone.0116829

Abstract

Population genetics models predict that the X (or Z) chromosome will evolve at faster rates than the autosomes in XY (or ZW) systems. Studies of molecular evolution using large datasets in multiple species have provided evidence supporting this faster-X effect in protein-coding sequences and, more recently, in transcriptomes. However, X-linked and autosomal genes differ significantly in important properties besides hemizygosity in males, including gene expression levels, tissue specificity in gene expression, and the number of interactions in which they are involved (i.e., protein-protein or DNA-protein interactions). Most important, these properties are known to correlate with rates of evolution, which raises the question of whether differences between the X chromosome and autosomes in gene properties, rather than hemizygosity, are sufficient to explain faster-X evolution. Here I investigate this possibility using whole genome sequences and transcriptomes of Drosophila yakuba and D. santomea and show that this is not the case. Additional factors are needed to account for faster-X evolution of both gene expression and protein-coding sequences beyond differences in gene properties, likely a higher incidence of positive selection in combination with the accumulation of weakly deleterious mutations.

Highlights

Population genetics theory predicts that under certain conditions the X chromosome will evolve at faster rates than the autosomes in XY systems, an effect known as faster-X [1,2]
To determine whether these properties are significantly associated with gene expression divergence in D. yakuba and D. santomea, I examined their distributions across the genome
Multiple-regression and nonparametric analyses indicate that faster-X is not the by-product of differences between X-linked and autosomal genes in properties known to correlate with rates of evolution, such as gene expression levels, tissue specificity in expression, and the number of protein interactions

Summary

Introduction

Population genetics theory predicts that under certain conditions the X chromosome will evolve at faster rates than the autosomes in XY (or ZW) systems, an effect known as faster-X [1,2]. In a population of diploids, newly arisen autosomal mutations are mostly found in heterozygotes and, if recessive for fitness, their effects are masked by the ancestral variants. If these mutations arise on the X chromosome and are beneficial, natural selection can drive them to fixation more efficiently because their fitness effects will be fully exposed in hemizygous males. Excess of Divergence in X-Linked Male-Biased Genes mutations at a faster rate than the autosomes. This difference is expected to be more extreme for mutations that affect only males [3]

Methods

Results

Conclusion