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Season-specific genetic variation underlies early-life migration in a partially migratory bird

Fortuna, Rita; Acker, Paul; Ugland, Cassandra R.; Burthe, Sarah J. ORCID: https://orcid.org/0000-0001-8871-3432; Harris, Michael P. ORCID: https://orcid.org/0000-0002-9559-5830; Newell, Mark A. ORCID: https://orcid.org/0000-0001-8875-2642; Gunn, Carrie; Morley, Timothy I.; Haaland, Thomas R.; Swann, Robert L.; Wanless, Sarah ORCID: https://orcid.org/0000-0002-2788-4606; Daunt, Francis ORCID: https://orcid.org/0000-0003-4638-3388; Reid, Jane M.. 2024 Season-specific genetic variation underlies early-life migration in a partially migratory bird. Proceedings of the Royal Society B: Biological Sciences, 291 (2033), 20241660. 12, pp. 10.1098/rspb.2024.1660

Abstract
Eco-evolutionary responses to environmentally induced selection fundamentally depend on magnitudes of genetic variation underlying traits that facilitate population persistence. Additive genetic variances and associated heritabilities can vary across environmental conditions, especially for labile phenotypic traits expressed through early life. However, short-term seasonal dynamics of genetic variances are rarely quantified in wild populations, precluding inference on eco-evolutionary outcomes in seasonally dynamic systems. This limitation applies to seasonal migration versus residence, constituting one key trait where rapid microevolution could rescue partially migratory populations from changing seasonal environments. We fitted novel quantitative genetic ‘capture–recapture animal models’ to multi-generational pedigree and year-round resighting data from 11 cohorts of European shags (Gulosus aristotelis), to estimate season-specific additive genetic variances in liabilities to migrate, and in resulting expression of migration, in juveniles’ first autumn and winter. We demonstrate non-negligible genetic variation underlying early-life migration, with twice as large additive genetic variances and heritabilities in autumn than winter. Since early-life survival selection on migration typically occurs in winter, highest genetic variation and strongest selection are seasonally desynchronized. Our results reveal complex within- and among-year dynamics of early-life genetic and phenotypic variation, demonstrating that adequate inference of eco-evolutionary outcomes requires quantifying microevolutionary potential on appropriate scales and seasonal timeframes.
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