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Keywords:

  • evolutionary strata;
  • Gasterosteus aculeatus ;
  • GC content;
  • genetic diversity;
  • pseudoautosomal region;
  • RAD sequencing;
  • sex chromosome

Abstract

Heterogeneity in recombination rate may strongly influence genome evolution and entail methodological challenges to genomic investigation. Nevertheless, a solid understanding of these issues awaits detailed information across a broad range of taxa. Based on 282 F2 individuals and 1872 single nucleotide polymorphisms, we characterize recombination in the threespine stickleback fish genome. We find an average genome-wide recombination rate of 3.11 cm/Mb. Crossover frequencies are dramatically elevated in the chromosome peripheries as compared to the centres, and are consistent with one obligate crossover per chromosome (but not chromosome arm). Along the sex chromosome, we show that recombination is restricted to a small pseudoautosomal domain of c. 2 Mb, spanning only 10% of that chromosome. Comparing female to male RAD sequence coverage allows us to identify two discrete levels of degeneration on the Y chromosome, one of these ‘evolutionary strata’ coinciding with a previously inferred inverted region. Using polymorphism data from two young (<10 000 years old) ecologically diverged lake-stream population pairs, we demonstrate that recombination rate correlates with both the magnitude of allele frequency shifts between populations and levels of genetic diversity within populations. These associations reflect genome-wide heterogeneity in the influence of selection on linked sites. We further find a strong relationship between recombination rate and GC content, possibly driven by GC-biased gene conversion. Overall, we highlight that heterogeneity in recombination rate has profound consequences on genome evolution and deserves wider recognition in marker-based genomic analyses.