Similar rates of protein adaptation in Drosophila miranda and D. melanogaster, two species with different current effective population sizes

Abstract

Background: Adaptive protein evolution is common in several Drosophila species investigated. Some studies point to very weak selection operating on amino-acid mutations, with average selection intensities on the order of Nes approximately in D. melanogaster and D. simulans. Species with lower effective population sizes should undergo less adaptation since they generate fewer mutations and selection is ineffective on a greater proportion of beneficial mutations.

Results: Here I study patterns of polymorphism and divergence at 91 X-linked loci in D. miranda, a species with a roughly 5-fold smaller effective population size than D. melanogaster. Surprisingly, I find a similar fraction of amino-acid mutations being driven to fixation by positive selection in D. miranda and D. melanogaster. Genes with higher rates of amino-acid evolution show lower levels of neutral diversity, a pattern predicted by recurrent adaptive protein evolution. I fit a hitchhiking model to patterns of polymorphism in D. miranda and D. melanogaster and estimate an order of magnitude higher selection coefficients for beneficial mutations in D. miranda.

Conclusion: This analysis suggests that effective population size may not be a major determinant in rates of protein adaptation. Instead, adaptation may not be mutation-limited, or the distribution of fitness effects for beneficial mutations might differ vastly between different species or populations. Alternative explanation such as biases in estimating the fraction of beneficial mutations or slightly deleterious mutation models are also discussed.

Figure 1

Neutral diversity is reduced in fast evolving protein-coding genes. The level of synonymous diversity (π_s) is plotted against the rate of amino-acid evolution (K_a) at X-linked loci in D. miranda. The solid line represents the least squares fit to a recurrent hitchhiking model.

Figure 2

An excess of rare polymorphisms and reduced codon bias in fast evolving protein-coding genes. A. Tajima's D, a measure of the frequency distributions of mutations, is plotted against the rate of amino-acid evolution (K_a) at X-linked loci in D. miranda. B. The frequency of optimal codons (Fop) is plotted against the rate of amino-acid evolution (K_a).

Figure 3

The frequency of adaptive mutations (U) versus their strength, for large and small populations. Assuming a fixed distribution of selective effects of mutations (s), large populations will have fewer effectively neutral mutations u_n (light grey area) but more beneficial mutations u_ben (dark grey area), than smaller populations. The mean effect of a beneficial that can become fixed in the species will be larger in a smaller population.