Nascent evolution of recombination rate differences as a consequence of chromosomal rearrangements

PLoS Genet. 2023 Aug 7;19(8):e1010717. doi: 10.1371/journal.pgen.1010717. eCollection 2023 Aug.

Abstract

Reshuffling of genetic variation occurs both by independent assortment of chromosomes and by homologous recombination. Such reshuffling can generate novel allele combinations and break linkage between advantageous and deleterious variants which increases both the potential and the efficacy of natural selection. Here we used high-density linkage maps to characterize global and regional recombination rate variation in two populations of the wood white butterfly (Leptidea sinapis) that differ considerably in their karyotype as a consequence of at least 27 chromosome fissions and fusions. The recombination data were compared to estimates of genetic diversity and measures of selection to assess the relationship between chromosomal rearrangements, crossing over, maintenance of genetic diversity and adaptation. Our data show that the recombination rate is influenced by both chromosome size and number, but that the difference in the number of crossovers between karyotypes is reduced as a consequence of a higher frequency of double crossovers in larger chromosomes. As expected from effects of selection on linked sites, we observed an overall positive association between recombination rate and genetic diversity in both populations. Our results also revealed a significant effect of chromosomal rearrangements on the rate of intergenic diversity change between populations, but limited effects on polymorphisms in coding sequence. We conclude that chromosomal rearrangements can have considerable effects on the recombination landscape and consequently influence both maintenance of genetic diversity and efficiency of selection in natural populations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chromosome Aberrations*
  • Humans
  • Karyotype
  • Polymorphism, Genetic
  • Recombination, Genetic*

Grants and funding

This work was funded by the Swedish Research Council (VR research grant #019-04791 to N.B.). The authors acknowledge support from the National Genomics Infrastructure in Stockholm funded by Science for Life Laboratory, the Knut and Alice Wallenberg Foundation and the Swedish Research Council, and SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure. The project was also supported by NBIS/SciLifeLab long-term bioinformatics support (WABI; to N.B.). R.V. was supported by the Spanish government (Agencia Estatal de Investigación) through grant PID2019-107078GB-I00/MCIN/AEI/10.13039/501100011033. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.