Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters

Marie Louis; Petra Korlević; Milaja Nykänen; Frederick Archer; Simon Berrow; Andrew Brownlow; Eline D. Lorenzen; Joanne O’Brien; Klaas Post; Fernando Racimo; Emer Rogan; Patricia E. Rosel; Mikkel-Holger S. Sinding; Henry van der Es; Nathan Wales; Michael C. Fontaine; Oscar E. Gaggiotti; Andrew D. Foote

doi:10.1038/s41467-023-39532-z

Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters

Marie Louis^*, Petra Korlević, Milaja Nykänen, Frederick Archer, Simon Berrow, Andrew Brownlow, Eline D. Lorenzen, Joanne O’Brien, Klaas Post, Fernando Racimo, Emer Rogan, Patricia E. Rosel, Mikkel-Holger S. Sinding, Henry van der Es, Nathan Wales, Michael C. Fontaine, Oscar E. Gaggiotti, Andrew D. Foote^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	English
Article number	4020
Number of pages	13
Journal	Nature Communications
Volume	14
DOIs	https://doi.org/10.1038/s41467-023-39532-z
Publication status	Published - 18 Jul 2023

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Replication data and scripts for: Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters
Louis, M. (Creator), Korlević, P. (Creator), Nykänen, M. (Creator), Archer, F. (Creator), Berrow, S. (Creator), Brownlow, A. (Creator), Lorenzen, E. (Creator), O'Brien, J. (Creator), Post, K. (Creator), Racimo, F. (Creator), Rogan, E. (Creator), Rosel, P. (Creator), Sinding, M. (Creator), Van Der Es, H. (Creator), Wales, N. (Creator), Fontaine, M. C. (Creator), Gaggiotti, O. (Creator) & Foote, A. (Creator), DataSuds, 2023
DOI: 10.23708/dabawd
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Louis, M., Korlević, P., Nykänen, M., Archer, F., Berrow, S., Brownlow, A., Lorenzen, E. D., O’Brien, J., Post, K., Racimo, F., Rogan, E., Rosel, P. E., Sinding, M.-H. S., van der Es, H., Wales, N., Fontaine, M. C., Gaggiotti, O. E., & Foote, A. D. (2023). Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters. Nature Communications, 14, Article 4020. https://doi.org/10.1038/s41467-023-39532-z

@article{e67cbebf2fa24b76b8e6d776412e5b9d,

title = "Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters",

abstract = "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.",

author = "Marie Louis and Petra Korlevi{\'c} and Milaja Nyk{\"a}nen and Frederick Archer and Simon Berrow and Andrew Brownlow and Lorenzen, {Eline D.} and Joanne O{\textquoteright}Brien and Klaas Post and Fernando Racimo and Emer Rogan and Rosel, {Patricia E.} and Sinding, {Mikkel-Holger S.} and {van der Es}, Henry and Nathan Wales and Fontaine, {Michael C.} and Gaggiotti, {Oscar E.} and Foote, {Andrew D.}",

note = "Funding: Open access funding provided by Norwegian University of Science and Technology. 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. Contemporary sample DNA extractions were supported by People{\textquoteright}s Trust for Endangered Species and the sequencing costs were supported by the European Union{\textquoteright}s Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska- 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 Sk{\l}odowska-Curie grant agreement No. 663830 and the European Research Council grant agreement No. ERC-COG-101045346.",

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doi = "10.1038/s41467-023-39532-z",

language = "English",

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journal = "Nature Communications",

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Louis, M, Korlević, P, Nykänen, M, Archer, F, Berrow, S, Brownlow, A, Lorenzen, ED, O’Brien, J, Post, K, Racimo, F, Rogan, E, Rosel, PE, Sinding, M-HS, van der Es, H, Wales, N, Fontaine, MC, Gaggiotti, OE & Foote, AD 2023, 'Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters', Nature Communications, vol. 14, 4020. https://doi.org/10.1038/s41467-023-39532-z

TY - JOUR

T1 - Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters

AU - Louis, Marie

AU - Korlević, Petra

AU - Nykänen, Milaja

AU - Archer, Frederick

AU - Berrow, Simon

AU - Brownlow, Andrew

AU - Lorenzen, Eline D.

AU - O’Brien, Joanne

AU - Post, Klaas

AU - Racimo, Fernando

AU - Rogan, Emer

AU - Rosel, Patricia E.

AU - Sinding, Mikkel-Holger S.

AU - van der Es, Henry

AU - Wales, Nathan

AU - Fontaine, Michael C.

AU - Gaggiotti, Oscar E.

AU - Foote, Andrew D.

N1 - Funding: Open access funding provided by Norwegian University of Science and Technology. 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. 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.

PY - 2023/7/18

Y1 - 2023/7/18

N2 - 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.

AB - 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.

U2 - 10.1038/s41467-023-39532-z

DO - 10.1038/s41467-023-39532-z

M3 - Article

C2 - 37463880

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

M1 - 4020

ER -

Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters

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