Runs of homozygosity reveal past bottlenecks and contemporary inbreeding
across diverging island populations of a bird
Abstract
Genomes retain evidence of the demographic history and evolutionary
forces that have shaped populations. Across island systems, contemporary
patterns of genetic diversity reflect complex population demography,
including colonisation events, bottlenecks, gene flow and genetic drift.
Here, we investigate whether island founder events have prolonged
effects on genome-wide diversity and runs of homozygosity (ROH)
distributions, using whole genome resequencing from six populations
across three archipelagos of Berthelot’s pipit (Anthus
berthelotii) - a passerine which has undergone island speciation
relatively recently. Pairwise sequential Markovian coalescent (PSMC)
analyses estimated divergence from its sister species approximately two
million years ago. Results indicate that all Berthelot’s pipit
populations had shared ancestry until approximately 50,000 years ago,
when the Madeiran archipelago populations were founded, while the
Selvagens were colonised within the last 8,000 years. We identify
extensive long ROH (>1 Mb) in genomes in the most recently
colonised populations of Madeira and Selvagens which have experienced
sequential island founder events and population crashes. Population
expansion within the last 100 years may have eroded long ROH in the
Madeiran archipelago, resulting in a prevalence of short ROH
(<1 Mb). Extensive long and short ROH in the Selvagens
reflects strong recent inbreeding, small contemporary effective
population size and past bottleneck effects, with as much as 37.7% of
the autosomes comprised of ROH >250 kb in length. These
findings highlight the importance of demographic history, as well as
selection and genetic drift, in shaping contemporary patterns of genomic
diversity across diverging populations.