Runs of homozygosity in killer whale genomes provide a global record of demographic histories

Andrew D. Foote*, Rebecca Hooper, Alana Alexander, Robin W. Baird, Charles Scott Baker, Lisa Ballance, Jay Barlow, Andrew Brownlow, Tim Collins, Rochelle Constantine, Luciano Dalla Rosa, Nicholas J. Davison, John W. Durban, Ruth Esteban, Laurent Excoffier, Sarah L. Fordyce Martin, Karin A. Forney, Tim Gerrodette, M. Thomas P. Gilbert, Christophe GuinetM. Bradley Hanson, Songhai Li, Michael D. Martin, Kelly M. Robertson, Filipa I. P. Samarra, Renaud de Stephanis, Sara B. Tavares, Paul Tixier, John A. Totterdell, Paul Wade, Jochen B. W. Wolf, Guangyi Fan, Yaolei Zhang, Phillip A. Morin

*Corresponding author for this work

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Abstract

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.

Original languageEnglish
JournalMolecular Ecology
Volume30
Issue number23
Pages (from-to)6162-6177
Number of pages16
ISSN0962-1083
DOIs
Publication statusPublished - 2021

Bibliographical note

Publisher Copyright:
© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Keywords

  • Demography
  • inbreeding
  • killer whale
  • Orcinus orca
  • Runs of Homozygosity
  • whole genome sequencing

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