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Mol Biol Evol. 2016 Feb;33(2):442-55. doi: 10.1093/molbev/msv236. Epub 2015 Oct 22.

Adaptive Evolution Is Substantially Impeded by Hill-Robertson Interference in Drosophila.

Author information

1
Genomics, Bioinformatics and Evolution Group, Institut de Biotecnologia i de Biomedicina (IBB) and Department de Genètica i Microbiologia, Campus Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain castellanoed@runbox.com a.c.eyre-walker@sussex.ac.uk.
2
Genomics, Bioinformatics and Evolution Group, Institut de Biotecnologia i de Biomedicina (IBB) and Department de Genètica i Microbiologia, Campus Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain.
3
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom.
4
Centre for the Study of Evolution, School of Life Sciences, University of Sussex, Brighton, United Kingdom castellanoed@runbox.com a.c.eyre-walker@sussex.ac.uk.

Abstract

Hill-Robertson interference (HRi) is expected to reduce the efficiency of natural selection when two or more linked selected sites do not segregate freely, but no attempt has been done so far to quantify the overall impact of HRi on the rate of adaptive evolution for any given genome. In this work, we estimate how much HRi impedes the rate of adaptive evolution in the coding genome of Drosophila melanogaster. We compiled a data set of 6,141 autosomal protein-coding genes from Drosophila, from which polymorphism levels in D. melanogaster and divergence out to D. yakuba were estimated. The rate of adaptive evolution was calculated using a derivative of the McDonald-Kreitman test that controls for slightly deleterious mutations. We find that the rate of adaptive amino acid substitution at a given position of the genome is positively correlated to both the rate of recombination and the mutation rate, and negatively correlated to the gene density of the region. These correlations are robust to controlling for each other, for synonymous codon bias and for gene functions related to immune response and testes. We show that HRi diminishes the rate of adaptive evolution by approximately 27%. Interestingly, genes with low mutation rates embedded in gene poor regions lose approximately 17% of their adaptive substitutions whereas genes with high mutation rates embedded in gene rich regions lose approximately 60%. We conclude that HRi hampers the rate of adaptive evolution in Drosophila and that the variation in recombination, mutation, and gene density along the genome affects the HRi effect.

KEYWORDS:

Drosophila; Hill–Robertson; adaptation; gene density; mutation; recombination

PMID:
26494843
PMCID:
PMC4794616
DOI:
10.1093/molbev/msv236
[Indexed for MEDLINE]
Free PMC Article

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