Abstract
Through an analysis of polymorphism within and divergence between species, we can hope to learn about the distribution of selective effects of mutations in the genome, changes in the fitness landscape that occur over time, and the location of sites involved in key adaptations that distinguish modern-day species. We introduce a novel method for the analysis of variation in selection pressures within and between species, spatially along the genome and temporally between lineages. We model codon evolution explicitly using a joint population genetics-phylogenetics approach that we developed for the construction of multiallelic models with mutation, selection, and drift. Our approach has the advantage of performing direct inference on coding sequences, inferring ancestral states probabilistically, utilizing allele frequency information, and generalizing to multiple species. We use a Bayesian sliding window model for intragenic variation in selection coefficients that efficiently combines information across sites and captures spatial clustering within the genome. To demonstrate the utility of the method, we infer selective pressures acting in Drosophila melanogaster and D. simulans from polymorphism and divergence data for 100 X-linked coding regions.
Highlights
The role of adaptation versus alternative, non-adaptive forces in shaping the diversity of life within and between species lies at the heart of many questions in biology [1,2,3]
We report the results of our analysis: the estimated distribution of fitness effects, the influence of sliding window length on what we learn about selection, examples of the local signal of variation in selection pressure, and broad patterns in the correlation in selection pressures along the genome and across evolutionary lineages
Our method has a number of advantages over predominantly population genetics-based approaches [18,20,38,39,42,43]
Summary
The role of adaptation versus alternative, non-adaptive forces in shaping the diversity of life within and between species lies at the heart of many questions in biology [1,2,3]. Detecting the genetic signature of natural selection in patterns of polymorphism and divergence across multiple species has become a major goal of evolutionary biology [4,5]. The McDonald-Kreitman (MK) test [16] exploits this contrast to detect adaptation where divergence or polymorphism data alone might not allow one to do so, owing to variation in selection coefficients within a gene. If adaptive change occurs at a limited number of sites in an otherwise constrained gene, deleterious mutations might limit the relative rate of nonsynonymous to synonymous substitution, DN/DS, to a value much less than 1, and thereby swamp the signal of adaptation. An excess DN/DS ratio compared to the relative rate of nonsynonymous to synonymous polymorphism, PN/PS, may still reveal a surplus of non-synonymous substitution compared to polymorphism, indicative of adaptive change. The MK test is a test of the null hypothesis, under the neutral theory [3,17], that the odds ratio (DN PS)/(DS PN) equals one; a DN/DS ratio significantly greater than PN/PS is indicative of adaptive evolution between the two species
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