The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster

José L Campos, Daniel L Halligan, Penelope R Haddrill, Brian Charlesworth

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Abstract

Genetic recombination associated with sexual reproduction increases the efficiency of natural selection by reducing the strength of Hill-Robertson interference. Such interference can be caused either by selective sweeps of positively selected alleles or by background selection (BGS) against deleterious mutations. Its consequences can be studied by comparing patterns of molecular evolution and variation in genomic regions with different rates of crossing over. We carried out a comprehensive study of the benefits of recombination in Drosophila melanogaster, both by contrasting five independent genomic regions that lack crossing over with the rest of the genome and by comparing regions with different rates of crossing over, using data on DNA sequence polymorphisms from an African population that is geographically close to the putatively ancestral population for the species, and on sequence divergence from a related species. We observed reductions in sequence diversity in noncrossover (NC) regions that are inconsistent with the effects of hard selective sweeps in the absence of recombination. Overall, the observed patterns suggest that the recombination rate experienced by a gene is positively related to an increase in the efficiency of both positive and purifying selection. The results are consistent with a BGS model with interference among selected sites in NC regions, and joint effects of BGS, selective sweeps, and a past population expansion on variability in regions of the genome that experience crossing over. In such crossover regions, the X chromosome exhibits a higher rate of adaptive protein sequence evolution than the autosomes, implying a Faster-X effect.

Original languageEnglish
Pages (from-to)1010-1028
Number of pages19
JournalMolecular Biology and Evolution
Volume31
Issue number4
DOIs
Publication statusPublished - Apr 2014

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Keywords

  • Drosophila melanogaster
  • crossing over
  • recombination
  • heterochromatin
  • Hill–Robertson interference
  • background selection
  • selective sweeps

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