Selection can favor a recombination landscape that limits polygenic adaptation

Meiotic crossover positions are uneven along eukaryotic chromosomes, giving rise to heterogeneous recombination rate landscapes. Genetic modifiers of local and genome-wide crossover positions have been described, but the selective pressures acting on them and their potential effect on adaptation in already-recombining populations remain unclear. We performed experimental evolution using a mutant that modifies the position of crossovers along chromosomes in the nematode Caenorhabditis elegans, without any detectable direct fitness effect. Our results show that when the recombination landscape is fixed, adaptation is facilitated by the modifier allele that, on average, increases recombination rates in genomic regions containing heritable fitness variation. However, in polymorphic populations containing both the wild-type and mutant modifier alleles, the allele that facilitates adaptation tends to decrease in frequency. This is likely because the allele that reduces recombination between selected loci at the genome-wide scale increases recombination in its chromosomal vicinity, and may thus benefit from local associations it establishes with beneficial genotype combinations. These results demonstrate that indirect selection acting on a recombination modifier mainly depends on its local effect, which may be decoupled from its consequences on genome-wide polygenic adaptation.