Range-wide genomic analysis reveals regional and meta-population dynamics of decline and recovery in the grey seal

Abstract

Funding: The work was supported by the Velux Foundations to M.T.O. (grant 123012), the BONUS BaltHealth project awarded to A.G., R.D. and M.T.O.funded jointly by the EU (Art. 185), the Innovation Fund Denmark (grant 6180- 00001B and 6180- 00002B), the Academy of Finland (grant 311966), theSwedish Foundation for Strategic Environmental Research (MISTRA), the American Scandinavian Foundation, and NIH/NIAID Centers of Excellence forInfluenza Research and Surveillance (HHSN272201400008C), and UK Natural Environment Research Council (NE/R015007/1). M.L.M. was supported bya Marie Skłodowska- Curie Actions TALENT programme fellowship (grant 801199), as well as a Carlsberg Foundation Semper Ardens Accelerate fellowshipto M.T.O. (grant CF21- 0425).Wildlife populations globally have experienced widespread historical declines due to anthropogenic and environmental impacts, yet for some species, contemporary management and conservation programmes have enabled recent recovery. The impacts of decline and recovery on genomic diversity and, vice versa, the genetic factors that contribute to conservation success or failure are rich areas for inquiry, with implications for shaping how we manage species into the future. To comprehensively characterise these processes in natural systems requires range-wide sampling and international collaboration, particularly for species with wide dispersal capabilities, broad geographic distributions, and complex regional metapopulation dynamics. Here, we present the first range- and genome-wide population genomic analysis of grey seals based on 3812 nuclear SNPs genotyped in 188 samples from 17 localities. Our analyses support the existence of three main grey seal populations centred in the NW Atlantic, NE Atlantic and Baltic Sea, and point to the existence of previously unrecognised substructure within the NE Atlantic. We detected remarkably low levels of genetic diversity in the NW Atlantic population, and demographic analyses revealed a turbulent history of NE Atlantic and Baltic Sea grey seals, with bottlenecks in the Middle Ages and the 20th century due to hunting and habitat alterations. We found some localities deviated from isolation by distance patterns, likely reflecting wide-scale metapopulation dynamics associated with recolonisation and recovery in regions where they were historically extirpated. We identify at least six grey seal genetic populations and reveal marked genetic effects of past declines and recent recovery across the species' range.Peer reviewe