Molecular evolution in nonrecombining regions of the Drosophila melanogaster genome

Abstract

We study the evolutionary effects of reduced recombination on the Drosophila melanogaster genome, analyzing more than 200 new genes that lack crossing-over and employing a novel orthology search among species of the melanogaster subgroup. These genes are located in the heterochromatin of chromosomes other than the dot (fourth) chromosome. Noncrossover regions of the genome all exhibited an elevated level of evolutionary divergence from D. yakuba at nonsynonymous sites, lower codon usage bias, lower GC content in coding and noncoding regions, and longer introns. Levels of gene expression are similar for genes in regions with and without crossing-over, which rules out the possibility that the reduced level of adaptation that we detect is caused by relaxed selection due to lower levels of gene expression in the heterochromatin. The patterns observed are consistent with a reduction in the efficacy of selection in all regions of the genome of D. melanogaster that lack crossing-over, as a result of the effects of enhanced Hill-Robertson interference. However, we also detected differences among nonrecombining locations: The X chromosome seems to exhibit the weakest effects, whereas the fourth chromosome and the heterochromatic genes on the autosomes located most proximal to the centromere showed the largest effects. However, signatures of selection on both nonsynonymous mutations and on codon usage persist in all heterochromatic regions.

FIG. 1.—

Notched box-plots of K_A, K_S, and K_A/K_S for: RA, recombining autosomal genes; RX, recombining X chromosome genes; No, nonfourth nonrecombining genes; N4, fourth chromosome genes; and NX, nonrecombining X chromosome genes. The box extends from the lower to the upper quartile, with a line in the middle at the median. The dotted bars represent the 5th and 95th percentiles. The notches represent 95% CIs for the medians.

FIG. 2.—

GC content of the third position of codons (GC₃), short introns (GC_S), and long introns (GC_L) for: RA, recombining autosomal genes; RX, recombining X chromosome genes; NoB, nonfourth beta-heterochromatin genes; NoA, nonfourth alpha-heterochromatin genes; N4, fourth chromosome genes; and NX, nonrecombining X chromosome genes. Values reported are means; error bars indicate 95% CIs obtained by bootstrapping.