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The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak," "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22–33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein–protein interactions, but not Hill–Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution. [ABSTRACT FROM AUTHOR]

Abstract: Theoretical work suggests that sexual conflict should promote the maintenance of genetic diversity by the opposing directions of selection on males and females. If such conflict is pervasive, it could potentially lead to genomic heterogeneity in levels of genetic diversity an idea that so far has not been empirically tested on a genomewide scale. We used large‐scale population genomic and transcriptomic data from the collared flycatcher (Ficedula albicollis) to analyse how sexual conflict, for which we use sex‐biased gene expression as a proxy, relates to genetic variability. Here, we demonstrate that the extent of sex‐biased gene expression of both male‐biased and female‐biased genes is significantly correlated with levels of nucleotide diversity in gene sequences and that this correlation extends to diversity levels also in intergenic DNA and introns. We find signatures of balancing selection in sex‐biased genes but also note that relaxed purifying selection could potentially explain part of the observed patterns. The finding of significant genetic differentiation between males and females for male‐biased (and gonad‐specific) genes indicates ongoing sexual conflict and sex‐specific viability selection, potentially driven by sexual selection. Our results thus indicate that sexual antagonism could potentially be considered as one viable explanation to the long‐standing question in evolutionary biology of how genomes can remain so genetically variable in face of strong natural and sexual selection. [ABSTRACT FROM AUTHOR]

The ratio of nonsynonymous to synonymous substitution rates (ω) is often used to measure the strength of natural selection. However, ω may be influenced by linkage among different targets of selection, that is, Hill–Robertson interference (HRI), which reduces the efficacy of selection. Recombination modulates the extent of HRI but may also affect ω by means of GC-biased gene conversion (gBGC), a process leading to a preferential fixation of G:C (“strong,” S) over A:T (“weak,” W) alleles. As HRI and gBGC can have opposing effects on ω, it is essential to understand their relative impact to make proper inferences of ω. We used a model that separately estimated S-to-S, S-to-W, W-to-S, and W-to-W substitution rates in 8,423 avian genes in the Ficedula flycatcher lineage. We found that the W-to-S substitution rate was positively, and the S-to-W rate negatively, correlated with recombination rate, in accordance with gBGC but not predicted by HRI. The W-to-S rate further showed the strongest impact on both dN and dS. However, since the effects were stronger at 4-fold than at 0-fold degenerated sites, likely because the GC content of these sites is farther away from its equilibrium, ω slightly decreases with increasing recombination rate, which could falsely be interpreted as a consequence of HRI. We corroborated this hypothesis analytically and demonstrate that under particular conditions, ω can decrease with increasing recombination rate. Analyses of the site-frequency spectrum showed that W-to-S mutations were skewed toward high, and S-to-W mutations toward low, frequencies, consistent with a prevalent gBGC-driven fixation bias. [ABSTRACT FROM AUTHOR]