Abstract
Recombination confers a major evolutionary advantage by breaking up linkage disequilibrium between harmful and beneficial mutations, thereby facilitating selection. However, in species that are only periodically sexual, such as many microbial eukaryotes, the realized rate of recombination is also affected by the frequency of sex, meaning that infrequent sex can increase the effects of selection at linked sites despite high recombination rates. Despite this, the rate of sex of most facultatively sexual species is unknown. Here, we use genomewide patterns of linkage disequilibrium to infer fine-scale recombination rate variation in the genome of the facultatively sexual green alga Chlamydomonas reinhardtii. We observe recombination rate variation of up to two orders of magnitude and find evidence of recombination hotspots across the genome. Recombination rate is highest flanking genes, consistent with trends observed in other nonmammalian organisms, though intergenic recombination rates vary by intergenic tract length. We also find a positive relationship between nucleotide diversity and physical recombination rate, suggesting a widespread influence of selection at linked sites in the genome. Finally, we use estimates of the effective rate of recombination to calculate the rate of sex that occurs in natural populations, estimating a sexual cycle roughly every 840 generations. We argue that the relatively infrequent rate of sex and large effective population size creates a population genetic environment that increases the influence of selection on linked sites across the genome.
Highlights
Recombination, the shuffling of existing genetic material, is both a fundamental evolutionary process and required to ensure proper disjunction of chromosomes during meiosis
We investigated for the presence of recombination hotspots, defining a hotspot as a region that was 1) >2 kb in length and 2) exhibited a >5-fold increase in ρLD as compared to the surrounding 80 kb of sequence on either side, following previous hotspot definitions (Singhal et al, 2015)
We find an enrichment of recombination hotspots within 2 kb of genes that leads to an overall increase in recombination rate surrounding genes, in concordance with observations in a number of other PR domain-containing 9 (PRDM9)-lacking organisms
Summary
Recombination, the shuffling of existing genetic material, is both a fundamental evolutionary process and required to ensure proper disjunction of chromosomes during meiosis. Meiotic recombination has two possible outcomes: crossing over (CO). There is clear evidence that recombination rate varies at multiple scales across nature, with variability observed within and between taxa as well as within the genome (Stapley et al., 2017). Recombination reduces interference between linked adaptive and harmful mutations and is an important determinant of how well natural selection can act. The spatial heterogeneity of recombination within genomes means that local recombination rate is an important determinant of the efficacy of selection and other evolutionary processes in a given genomic region (Hill and Robertson, 1966, Felsenstein, 1974, McVean et al, 2004). Understanding the predictors of recombination rate variation has constituted a core objective in the study of how recombination affects genome evolution
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