The roles of recombination and selection in shaping genomic divergence in an incipient ecological species complex

Mol Ecol. 2023 Mar;32(6):1478-1496. doi: 10.1111/mec.16383. Epub 2022 Feb 15.

Abstract

Speciation genomic studies have revealed that genomes of diverging lineages are shaped jointly by the actions of gene flow and selection. These evolutionary forces acting in concert with processes such as recombination and genome features such as gene density shape a mosaic landscape of divergence. We investigated the roles of recombination and gene density in shaping the patterns of differentiation and divergence between the cyclically parthenogenetic ecological sister-taxa, Daphnia pulicaria and Daphnia pulex. First, we assembled a phased chromosome-scale genome assembly using trio-binning for D. pulicaria and constructed a genetic map using an F2-intercross panel to understand sex-specific recombination rate heterogeneity. Finally, we used a ddRADseq data set with broad geographic sampling of D. pulicaria, D. pulex, and their hybrids to understand the patterns of genome-scale divergence and demographic parameters. Our study provides the first sex-specific estimates of recombination rates for a cyclical parthenogen, and unlike other eukaryotic species, we observed male-biased heterochiasmy in D. pulicaria, which may be related to this somewhat unique breeding mode. Additionally, regions of high gene density and recombination are generally more divergent than regions of suppressed recombination. Outlier analysis indicated that divergent genomic regions are probably driven by selection on D. pulicaria, the derived lineage colonizing a novel lake habitat. Together, our study supports a scenario of selection acting on genes related to local adaptation shaping genome-wide patterns of differentiation despite high local recombination rates in this species complex. Finally, we discuss the limitations of our data in light of demographic uncertainty.

Keywords: Daphnia; Pacific Biosciences HiFi; genetic linkage map; genome assembly; recombination; speciation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acclimatization*
  • Animals
  • Biological Evolution
  • Daphnia / genetics
  • Female
  • Genomics*
  • Male
  • Recombination, Genetic / genetics