Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters

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Parallel evolution provides strong evidence of adaptation by natural selection due to local environmental variation. Yet, the chronology, and mode of the process of parallel evolution remains debated. Here, we harness the temporal resolution of paleogenomics to address these long-standing questions, by comparing genomes originating from the mid-Holocene (8610-5626 years before present, BP) to contemporary pairs of coastal-pelagic ecotypes of bottlenose dolphin. We find that the affinity of ancient samples to coastal populations increases as the age of the samples decreases. We assess the youngest genome (5626 years BP) at sites previously inferred to be under parallel selection to coastal habitats and find it contained coastal-associated genotypes. Thus, coastal-associated variants rose to detectable frequencies close to the emergence of coastal habitat. Admixture graph analyses reveal a reticulate evolutionary history between pelagic and coastal populations, sharing standing genetic variation that facilitated rapid adaptation to newly emerged coastal habitats.

OriginalsprogEngelsk
Artikelnummer4020
TidsskriftNature Communications
Vol/bind14
Antal sider13
ISSN2041-1723
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
We especially thank Matthias Meyer for providing the SP1060 library, which allowed the generation of the ancient genome that was central to this study. We thank Ramon Fallon, Joseph Ward and Peter Thorpe from the St Andrews Bioinformatics Unit for help with bioinformatics. Bioinformatics and computational analyses were supported by the University of St Andrews Bioinformatics Unit which is funded by a Wellcome Trust ISSF award [grant 105621/Z/14/Z] and ran on cluster marvin and Crop Diversity HPC. We thank Kelly Roberston for the laboratory work for the contemporary samples from the USA and for arranging shipment. We thank M. Thomas P. Gilbert for our use of the ancient DNA facilities in Copenhagen. We thank Jazmín Ramos Madrigal for advice on data format conversion. We thank everyone involved in sample collection including Conor Ryan for sampling some of the stranded individuals in Ireland, the stranding networks in Ireland and Scotland and the Groupe d’Etude des Cétacés du Cotentin, and the NOAA Southeast and Southwest Fisheries Science Centre field crews and Simon Ingram for biopsy sample collection. Funding for ancient DNA labwork and sequencing was provided by the Total Foundation awarded to M.L. Funding for sample collection in Ireland was provided by Science Foundation Ireland. Funding for labwork and visits to the University of Copenhagen was provided by the Systematics Research Fund, a Godfrey Hewitt mobility award from the European Society for Evolutionary Biology (ESEB), Lerner- Gray Grants for Marine Research. M.L. was supported by a Fyssen Fellowship, Total Foundation, the University of St Andrews and the Greenland Research Council. Contemporary sample DNA extractions were supported by People’s Trust for Endangered Species and the sequencing costs were supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 663830 awarded to A.D.F., by the Total Foundation awarded to M.L., the University of Groningen awarded to M.C.F., and the Marine Alliance for Science and Technology for Scotland and The Russell Trust awarded to O.E.G. M.N. was funded by MASTS and the Crawford Hayes fund. A.D.F. was funded by Marie Skłodowska-Curie grant agreement No. 663830 and the European Research Council grant agreement No. ERC-COG-101045346.

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© 2023, The Author(s).

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