Heterogeneous evolution of effective recombination landscapes across percomorph fishes

Abstract

Recombination shapes allelic combinations across the genome and plays a central role in adaptation and speciation. While recombination rates are known to vary and evolve, how recombination landscapes diverge between populations and which processes drive this divergence remains poorly understood. Here, we use the Population Recombination Divergence Index (PRDI) to quantify divergence in effective recombination landscapes between seven pairs of populations and species from four percomorph fish lineages (cichlids, sticklebacks, killifish, and clownfish). While accounting for stochasticity and confounders of linkage disequilibrium (LD) -based recombination rate estimates, we find that recombination landscapes diverged substantially in all comparisons. This divergence generally increases with genetic differentiation and divergence time, but the amount of PRDI accumulated per unit of genetic divergence (FST), net nucleotide divergence (da), or divergence time varies markedly among population and species pairs. Comparisons across systems suggest that PRDI accumulation tends to be faster (per unit of FST, da, or divergence time) in pairs with higher inferred gene flow. We also introduce a local version of PRDI (_l) to better characterize genomic heterogeneity in effective recombination divergence. We find that higher inferred gene flow between populations tends to be associated with stronger intragenomic correlation between local FST and _l. Finally, we propose a conceptual framework for investigating how divergent selection and gene flow may interact to shape effective recombination landscape divergence. Our work highlights the heterogeneous dynamics of effective recombination landscape evolution, and motivates further theoretical and empirical efforts to integrate recombination landscape evolution into studies of adaptation and speciation.