Drivers of linkage disequilibrium across a species' geographic range

PLoS Genet. 2021 Mar 26;17(3):e1009477. doi: 10.1371/journal.pgen.1009477. eCollection 2021 Mar.

Abstract

While linkage disequilibrium (LD) is an important parameter in genetics and evolutionary biology, the drivers of LD remain elusive. Using whole-genome sequences from across a species' range, we assessed the impact of demographic history and mating system on LD. Both range expansion and a shift from outcrossing to selfing in North American Arabidopsis lyrata were associated with increased average genome-wide LD. Our results indicate that range expansion increases short-distance LD at the farthest range edges by about the same amount as a shift to selfing. However, the extent over which LD in genic regions unfolds was shorter for range expansion compared to selfing. Linkage among putatively neutral variants and between neutral and deleterious variants increased to a similar degree with range expansion, providing support that genome-wide LD was positively associated with mutational load. As a consequence, LD combined with mutational load may decelerate range expansions and set range limits. Finally, a small number of genes were identified as LD outliers, suggesting that they experience selection by either of the two demographic processes. These included genes involved in flowering and photoperiod for range expansion, and the self-incompatibility locus for mating system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Biological Evolution
  • Drosophila Proteins
  • Genetic Variation*
  • Genome, Plant
  • Genomics / methods
  • Linkage Disequilibrium*
  • Phylogeography
  • Polymorphism, Single Nucleotide
  • Recombination, Genetic

Substances

  • Drosophila Proteins

Grants and funding

This study was funded by the Swiss National Science Foundation, Grant Number: PP00P3_123396, PP00P3_146342, 31003A_140979 and 31003A_166322 to YW; and Fondation Pierre Mercier pour la Science, Lausanne to YW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.