Abstract
Recombination reshuffles the alleles of a population through crossover and gene conversion. These mechanisms have considerable consequences on the evolution and maintenance of genetic diversity. Crossover, for example, can increase genetic diversity by breaking the linkage between selected and nearby neutral variants. Bias in favor of G or C alleles during gene conversion may instead promote the fixation of one allele over the other, thus decreasing diversity. Mutation bias from G or C to A and T opposes GC-biased gene conversion (gBGC). Less recognized is that these two processes may—when balanced—promote genetic diversity. Here, we investigate how gBGC and mutation bias shape genetic diversity patterns in wood white butterflies (Leptidea sp.). This constitutes the first in-depth investigation of gBGC in butterflies. Using 60 resequenced genomes from six populations of three species, we find substantial variation in the strength of gBGC across lineages. When modeling the balance of gBGC and mutation bias and comparing analytical results with empirical data, we reject gBGC as the main determinant of genetic diversity in these butterfly species. As alternatives, we consider linked selection and GC content. We find evidence that high values of both reduce diversity. We also show that the joint effects of gBGC and mutation bias can give rise to a diversity pattern which resembles the signature of linked selection. Consequently, gBGC should be considered when interpreting the effects of linked selection on levels of genetic diversity.
Highlights
The neutral theory of molecular evolution postulates that the majority of genetic differences within and between species are due to selectively neutral variants (Kimura 1983; Jensen et al 2019)
We highlight that GC-biased gene conversion (gBGC) is a pervasive force, influencing rates and patterns of molecular evolution both among and across the genomes of Leptidea butterflies
We further emphasize that gBGC shapes genetic diversity and may—through fixation of weak to strong (W!S) mutations—lead to a concomitant increase in diversity if opposed by a strong to weak (S!W) mutation bias. This means that positive correlations between genetic diversity and recombination do not necessarily imply that selection is affecting diversity in the genome
Summary
The neutral theory of molecular evolution postulates that the majority of genetic differences within and between species are due to selectively neutral variants (Kimura 1983; Jensen et al 2019). Lewontin (1974) noted that the range of observed values of Ne estimated from genetic diversity measures is smaller than the range of census population sizes, Nc (Lewontin’s paradox; Lewontin 1974; Kimura 1983; Nevo et al 1984; Frankham 1995).
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