Abstract
In Drosophila, multiple lines of evidence converge in suggesting that beneficial substitutions to the genome may be common. All suffer from confounding factors, however, such that the interpretation of the evidence—in particular, conclusions about the rate and strength of beneficial substitutions—remains tentative. Here, we use genome-wide polymorphism data in D. simulans and sequenced genomes of its close relatives to construct a readily interpretable characterization of the effects of positive selection: the shape of average neutral diversity around amino acid substitutions. As expected under recurrent selective sweeps, we find a trough in diversity levels around amino acid but not around synonymous substitutions, a distinctive pattern that is not expected under alternative models. This characterization is richer than previous approaches, which relied on limited summaries of the data (e.g., the slope of a scatter plot), and relates to underlying selection parameters in a straightforward way, allowing us to make more reliable inferences about the prevalence and strength of adaptation. Specifically, we develop a coalescent-based model for the shape of the entire curve and use it to infer adaptive parameters by maximum likelihood. Our inference suggests that ∼13% of amino acid substitutions cause selective sweeps. Interestingly, it reveals two classes of beneficial fixations: a minority (approximately 3%) that appears to have had large selective effects and accounts for most of the reduction in diversity, and the remaining 10%, which seem to have had very weak selective effects. These estimates therefore help to reconcile the apparent conflict among previously published estimates of the strength of selection. More generally, our findings provide unequivocal evidence for strongly beneficial substitutions in Drosophila and illustrate how the rapidly accumulating genome-wide data can be leveraged to address enduring questions about the genetic basis of adaptation.
Highlights
A central challenge of evolutionary biology is to elucidate the nature of adaptive changes to the genome: do they comprise a negligible or substantial fraction of differences among species? When they occur, are they driven by strong positive selection or are they fine-tunings of minor consequence to fitness? In Drosophila, perhaps the most studied taxon in these respects, there are conflicting accounts regarding the intensity of selection driving adaptations [1,2,3,4] but accumulating lines of evidence suggest that adaptation may be prevalent [5,6,7]
When a rare or new allele is favored and fixes in the population, it drags closely linked neutral alleles to loss or fixation. This ‘‘selective sweep’’ leads to a transient reduction in levels of neutral diversity around a beneficial substitution, where the size of the affected region decreases with the recombination rate and increases with the intensity of positive selection [18,19,20]
In order to teach us about adaptive evolution, these footprints need to be specific to positive selection as well as rich enough to allow for reliable inferences
Summary
A central challenge of evolutionary biology is to elucidate the nature of adaptive changes to the genome: do they comprise a negligible or substantial fraction of differences among species? When they occur, are they driven by strong positive selection or are they fine-tunings of minor consequence to fitness? In Drosophila, perhaps the most studied taxon in these respects, there are conflicting accounts regarding the intensity of selection driving adaptations [1,2,3,4] but accumulating lines of evidence suggest that adaptation may be prevalent [5,6,7]. Numerous studies based on extensions of this approach indicate that approximately one in two amino acid and one in five non-coding differences between Drosophila species may be adaptive [7,11,12,13,14] These findings remain tentative, because other factors, and notably plausible demographic scenarios, could cause a substantial overestimation of the fraction of beneficial substitutions [7,8,15,16,17]. When a rare or new allele is favored and fixes in the population, it drags closely linked neutral alleles to loss or fixation This ‘‘selective sweep’’ leads to a transient reduction in levels of neutral diversity around a beneficial substitution, where the size of the affected region decreases with the recombination rate and increases with the intensity of positive selection [18,19,20]. Previous studies relied on limited summaries of the data, thereby losing much of the information carried by the spatial signature of
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