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

SUMMARY Runs of homozygosity (ROH) occur when offspring receive the same ancestral haplotype from both parents, and, accordingly, reduce individual heterozygosity. Their distribution throughout the genome contains information on the probability of inbreeding mediated by mating system and population demography. Here, we investigate variation in killer whale demographic history as reflected in genome-wide heterozygosity, using a global dataset of 26 genomes. We find an overall pattern of lower heterozygosity in genomes sampled at high latitudes, with hundreds of short ROH (< 1Mbp) reflecting high background relatedness due to coalescence of haplotypes during bottlenecks associated with founder events during post-glacial range expansions. Across most of the species’ range, intermediate length ROH (1-10Mb) revealed long-term inbreeding in 22 of the 26 sampled killer whale genomes, consistent with the high social philopatry observed in all populations studied to date. Inbreeding coefficients (FROH) were comparable to those reported in other taxa with long-term low population size, such as bonobos and the Native American Karitiana of the Brazilian Amazon. The extreme outlier in this dataset, a Scottish killer whale, was homozygous over one-third of the autosomes (41.6%) with a distinct distribution of ROH length, indicating generations of inbreeding. This exceeds autozygosity in emblematic examples of long-term inbreeding, such as the Altai Neanderthal, and eastern lowland and mountain gorillas. The fate of this Scottish killer whale population, in which no calves have been born in over two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.