Demographic history and genomic consequences of 10,000 generations of isolation in a wild mammal.

Increased human activities caused the isolation of populations in many species—often associated with genetic depletion and negative fitness effects. The effects of isolation are predicted by theory, but long-term data from natural populations are scarce. We show, with full genome sequences, that common voles (Microtus arvalis) in the Orkney archipelago have remained genetically isolated from conspecifics in continental Europe since their introduction by humans over 5,000 years ago. Modern Orkney vole populations are genetically highly differentiated from continental conspecifics as a result of genetic drift processes. Colonization likely started on the biggest Orkney island and vole populations on smaller islands were gradually split off, without signs of secondary admixture. Despite having large modern population sizes, Orkney voles are genetically depauperate and successive introductions to smaller islands resulted in further reduction of genetic diversity. We detected high levels of fixation of predicted deleterious variation compared with continental populations, particularly on smaller islands, yet the fitness effects realized in nature are unknown. Simulations showed that predominantly mildly deleterious mutations were fixed in populations, while highly deleterious mutations were purged early in the history of the Orkney population. Relaxation of selection overall due to benign environmental conditions on the islands and the effects of soft selection may have contributed to the repeated, successful establishment of Orkney voles despite potential fitness loss. Furthermore, the specific life history of these small mammals, resulting in relatively large population sizes, has probably been important for their long-term persistence in full isolation. [Display omitted] • Common voles on Orkney remained completely isolated for more than 5,000 years • Genetic drift led to a strong reduction of genetic diversity and population divergence • Orkney voles have high levels of detrimental mutations, especially on small islands • Simulations suggest purging of highly deleterious alleles, while mild ones persisted Wang et al. show that common voles on the Orkney archipelago have remained genetically isolated for more than 5,000 years after human introduction. Orkney voles lost most genetic diversity and harbor high levels of inferred strongly deleterious mutations, yet simulations and large current population sizes suggest rather mild effects on fitness. [ABSTRACT FROM AUTHOR]