Population genomics of big mice from the Faroe islands: Hybridization, colonization, and a new challenge to identifying genomic targets of selection

Populations that colonize islands provide unique insights into demography,
adaptation, and the spread of invasive species. House mice on the Faroe
Islands evolved exceptionally large bodies after colonization, generating
interest from biologists going back to Darwin. To reconstruct the
evolutionary history of these mice, we sequenced genomes of population
samples from three Faroe Islands (Nolsoy, Sandoy, Mykines) and Norway as a
mainland comparison. Mice from the Faroe Islands are inferred to be
hybrids between the subspecies Mus musculus domesticus and M. m. musculus,
with ancestry alternating along the genome. The mice are predominantly M.
m. domesticus in origin, reflecting repeated backcrossing to this
subspecies following initial hybridization. Analyses based on the site
frequency spectrum of single nucleotide polymorphisms and the ancestral
recombination graph indicate that mice spread to the Faroe Islands on a
timescale consistent with dispersal by Norwegian Vikings, with
colonization of Sandoy likely preceding colonization of Nolsoy.
Substantial reductions in nucleotide diversity and effective population
size associated with colonization are inferred, raising the prospect that
mice on the Faroe Islands evolved large body size during periods of
heightened genetic drift. Genomic scans for positive selection uncover
windows with unusual site frequency spectra, but this pattern is mostly
generated by clusters of singletons in individual mice. Variants showing
evidence of selection based on the ancestral recombination graph in Nolsoy
and Sandoy are enriched for genes with neurological functions. Our
findings reveal a dynamic evolutionary history for the enigmatic mice from
Faroe Island and emphasize the challenges that accompany population
genomic inferences in island populations.