Leveraging Whole Genomes, Mitochondrial DNA and Haploblocks to Decipher Complex Demographic Histories: An Example From a Broadly Admixed Arctic Fish

Abstract

The study of phylogeography has transitioned from mitochondrial haplotypes to genome-wide analyses, borrowing from population genomics methods along the way. Whole-genome sequencing allows the study of both mitochondrial and nuclear DNA and provides the density of markers to investigate recombination along the genome. This level of resolution could unravel complex histories of admixture between lineages, which are commonly observed in species evolving in recently deglaciated habitats. In this study, we sequenced 1120 Arctic Char genomes from 33 populations across Canada and Greenland to characterise patterns of genetic variation and diversity, and how they are shaped by hybridisation between the Arctic and Atlantic glacial lineages. Mitochondrial genomes across the study area were predominantly of Arctic origin, except in Greenland, where we observed some Atlantic descent. Through admixture analyses and demographic inferences on nuclear markers, we identified that all Canadian populations under the 66th parallel showed introgression from the Atlantic lineage, leading to higher genetic diversity. By scanning the genome using local principal component analyses, we identified putative large low-recombining haploblocks as local ancestry tracts from either lineage. Since haplotypes might retain different signatures of postglacial histories by sheltering sequences from recombination, we attempted to infer origins of recolonisation using whole genomes vs. ancestry tracts for the Arctic lineage. Despite limitations, we unveiled clues suggesting a complex postglacial history in Arctic Char. Overall, our study demonstrates that, even at low depth, making the most of whole-genome sequencing by analysing several genomic compartments provides a versatile and powerful way to address phylogeographic dynamics.