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The Distribution and Dispersal of Large Haploblocks in a Superspecies

Irwin, Darren LU ; Bensch, Staffan LU orcid ; Charlebois, Caleigh ; David, Gabriel ; Geraldes, Armando ; Gupta, Sandeep Kumar ; Harr, Bettina ; Holt, Paul ; Irwin, Jessica H. LU and Ivanitskii, Vladimir V. , et al. (2025) In Molecular Ecology 34(21).
Abstract

Haploblocks are regions of the genome that coalesce to an ancestor as a single unit. Differentiated haplotypes in these regions can result from the accumulation of mutational differences in low-recombination chromosomal regions, especially when selective sweeps occur within geographically structured populations. We introduce a method to identify large well-differentiated haploblock regions (LHBRs), based on the variance in standardised heterozygosity (ViSHet) of single nucleotide polymorphism (SNP) genotypes among individuals, calculated across a genomic region (500 SNPs in our case). We apply this method to the greenish warbler (Phylloscopus trochiloides) ring species, using a newly assembled reference genome and genotypes at more than... (More)

Haploblocks are regions of the genome that coalesce to an ancestor as a single unit. Differentiated haplotypes in these regions can result from the accumulation of mutational differences in low-recombination chromosomal regions, especially when selective sweeps occur within geographically structured populations. We introduce a method to identify large well-differentiated haploblock regions (LHBRs), based on the variance in standardised heterozygosity (ViSHet) of single nucleotide polymorphism (SNP) genotypes among individuals, calculated across a genomic region (500 SNPs in our case). We apply this method to the greenish warbler (Phylloscopus trochiloides) ring species, using a newly assembled reference genome and genotypes at more than 1 million SNPs among 257 individuals. Most chromosomes carry a single distinctive LHBR, containing 4–6 distinct haplotypes that are associated with geography, enabling detection of hybridisation events and transition zones between differentiated populations. LHBRs have exceptionally low within-haplotype nucleotide variation and moderately low between-haplotype nucleotide distance, suggesting their establishment through recurrent selective sweeps at varying geographic scales. Meiotic drive is potentially a powerful mechanism of producing such selective sweeps, and the LHBRs are likely to often represent centromeric regions where recombination is restricted. Links between populations enable introgression of favoured haplotypes and we identify one haploblock showing a highly discordant distribution compared to most of the genome, being present in two distantly separated geographic regions that are at similar latitudes in both east and central Asia. Our results set the stage for detailed studies of haploblocks, including their genomic location, gene content and contribution to reproductive isolation.

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@article{542917ab-a653-4821-80ea-a979c2bf2278,
  abstract     = {{<p>Haploblocks are regions of the genome that coalesce to an ancestor as a single unit. Differentiated haplotypes in these regions can result from the accumulation of mutational differences in low-recombination chromosomal regions, especially when selective sweeps occur within geographically structured populations. We introduce a method to identify large well-differentiated haploblock regions (LHBRs), based on the variance in standardised heterozygosity (ViSHet) of single nucleotide polymorphism (SNP) genotypes among individuals, calculated across a genomic region (500 SNPs in our case). We apply this method to the greenish warbler (Phylloscopus trochiloides) ring species, using a newly assembled reference genome and genotypes at more than 1 million SNPs among 257 individuals. Most chromosomes carry a single distinctive LHBR, containing 4–6 distinct haplotypes that are associated with geography, enabling detection of hybridisation events and transition zones between differentiated populations. LHBRs have exceptionally low within-haplotype nucleotide variation and moderately low between-haplotype nucleotide distance, suggesting their establishment through recurrent selective sweeps at varying geographic scales. Meiotic drive is potentially a powerful mechanism of producing such selective sweeps, and the LHBRs are likely to often represent centromeric regions where recombination is restricted. Links between populations enable introgression of favoured haplotypes and we identify one haploblock showing a highly discordant distribution compared to most of the genome, being present in two distantly separated geographic regions that are at similar latitudes in both east and central Asia. Our results set the stage for detailed studies of haploblocks, including their genomic location, gene content and contribution to reproductive isolation.</p>}},
  author       = {{Irwin, Darren and Bensch, Staffan and Charlebois, Caleigh and David, Gabriel and Geraldes, Armando and Gupta, Sandeep Kumar and Harr, Bettina and Holt, Paul and Irwin, Jessica H. and Ivanitskii, Vladimir V. and Marova, Irina M. and Niu, Yongchao and Seneviratne, Sampath and Singh, Ashutosh and Wu, Yongjie and Zhang, Shangmingyu and Price, Trevor D.}},
  issn         = {{0962-1083}},
  keywords     = {{hybridization; Phylloscopus plumbeitarsus; Phylloscopus trochiloides; reproductive isolation; ring species; speciation}},
  language     = {{eng}},
  number       = {{21}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Ecology}},
  title        = {{The Distribution and Dispersal of Large Haploblocks in a Superspecies}},
  url          = {{http://dx.doi.org/10.1111/mec.17731}},
  doi          = {{10.1111/mec.17731}},
  volume       = {{34}},
  year         = {{2025}},
}