Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Abstract

AbstractMeiotic recombination is fundamental to evolution of sexually reproducing organisms and differences in recombination rates are important during rapid adaptation and organismal diversification. Many unknowns remain regarding how and why recombination landscapes evolve in nature. Here, we reconstruct recombination maps based on linkage disequilibrium and use subsampling and simulations to show that fine-scale recombination landscapes differ substantially between two cichlid fish ecotypes ofAstatotilapia callipterathat diverged only ∼2,500 generations ago. The observed results are not driven by PDRM9, whose binding sites do not show any relationship to recombination rates in this species. We show that regions where recombination histories differ between ecotypes have non-random distribution across chromosomes. They are associated with, but only partially explained, by regions of high divergence between ecotypes in allele frequency (FST) and / or nucleotide diversity. We also found 47 large haplotype blocks that are polymorphic in Lake Masoko, cover 21% of the genome, appear to include inversions, and contribute disproportionately to the evolution of recombination. Only a small number of them have elevatedFST. While some haplotype blocks are old and likely maintained by balancing selection, for most, the age of ancestry is close to the genome-wide average. Among haplotype blocks, there is a strong and clear association between the degree of recombination divergence and ecotype clustering by individual heterozygosity. Overall, our work provides a holistic view of changes in recombination landscapes during early stages of speciation with gene flow and advances our understanding of the combinatorial basis of evolution.