The recombination landscape of introgression in yeast

Abstract

Meiotic recombination is an important evolutionary force that acts by breaking up genomic linkage, thereby increasing the efficacy of selection. Meiotic recombination is initiated with a double-strand break which is resolved via a crossover, which involves the reciprocal exchange of genetic material between homologous chromosomes, or a non-crossover, which results in small tracts of non-reciprocal exchange of genetic material. While the meiotic process is largely conserved, crossover and non-crossover rates vary between species, populations, individuals, and across the genome. In recent years, recombination is observed to be positively associated with the distribution of ancestry derived from past interspecific hybridization (introgression) in a variety of species. This trend has been interpreted to signify that introgression carries genetic incompatibilities that are selected against, such that introgression is enriched in regions of high recombination. However, recombination is well known to be suppressed in divergent sequence to prevent non-homologous recombination. Since introgressed DNA is often divergent, we sought to explore this interaction of recombination and introgression by sequencing spores and detecting crossover and non-crossover events from two crosses of the budding yeast Saccharomyces uvarum . One cross is between strains isolated from natural environments, and the other cross is between strains from fermentation environments, in which each strain contains introgression from their sister species, S. eubayanus . We find that the recombination landscape is significantly different between S. uvarum crosses, and that most of these differences can be explained by the presence of heterozygous introgression in the fermentation cross. Crossovers are significantly reduced and non-crossovers are increased in heterozygous introgression compared to syntenic regions in the natural cross without introgression. This translates to reduced allele shuffling within introgressed regions, and an overall reduction of shuffling on most chromosomes with introgression compared to the syntenic regions and chromosomes without introgression. Our results indicate that recent hybridization can significantly influence the recombination landscape, and suggest that the reduction in allele shuffling contributes to the initial purging of introgressed ancestry in the generations following a hybridization event.