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

Andrew Foote 1, 2, 3 Rebecca Hooper 4 Alana Alexander 5 Robin Baird 6 Charles Scott Baker 7, 8 Lisa Ballance 7, 9 Jay Barlow 9 Andrew Brownlow 10 Tim Collins 11 Rochelle Constantine 8 Luciano Dalla Rosa 12 Nicholas Davison 10 John Durban 7, 9 Ruth Esteban 13 Laurent Excoffier 3 Sarah L. Fordyce Martin 1 Karin A. Forney 9, 14 Tim Gerrodette 9 M. Thomas P. Gilbert 1, 15 Christophe Guinet 16 M. Bradley Hanson 17 Songhai Li 18 Michael Martin 1 Kelly Robertson 9 Filipa I. P. Samarra 19 Renaud de Stephanis 13 Sara B. Tavares 20, 21 Paul Tixier 16, 22 John A. Totterdell 23 Paul Wade 24 Jochen B. W. Wolf 25 Guangyi Fan 26, 27, 28 Yaolei Zhang 26, 29 Phillip A. Morin 9 
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.
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Andrew Foote, Rebecca Hooper, Alana Alexander, Robin Baird, Charles Scott Baker, et al.. Runs of homozygosity in killer whale genomes provide a global record of demographic histories. Molecular Ecology, Wiley, 2021, 30, pp.6162-6177. ⟨10.1111/mec.16137⟩. ⟨hal-03346188⟩

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