Killer whale genomes reveal a complex history of recurrent admixture and vicariance

Andrew D Foote, Michael D Martin, Marie Louis, George Pacheco, Kelly M Robertson, Mikkel-Holger S Sinding, Ana R Amaral, Robin W Baird, Charles Scott Baker, Lisa Ballance, Jay Barlow, Andrew Brownlow, Tim Collins, Rochelle Constantine, Willy Dabin, Luciano Dalla Rosa, Nicholas J Davison, John W Durban, Ruth Esteban, Steven H FergusonTim Gerrodette, Christophe Guinet, M Bradley Hanson, Wayne Hoggard, Cory J D Matthews, Filipa I P Samarra, Renaud de Stephanis, Sara B Tavares, Paul Tixier, John A Totterdell, Paul Wade, Laurent Excoffier, M Thomas P Gilbert, Jochen B W Wolf, Phillip A Morin

Research output: Contribution to journalArticle

Abstract

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Original languageEnglish
Pages (from-to)3427-3444
Number of pages18
JournalMolecular Ecology
Volume28
Issue number14
Early online date27 May 2019
DOIs
Publication statusPrint publication - Jul 2019

Fingerprint

Killer Whale
Orcinus orca
vicariance
whale
genome
Genome
history
ancestry
Population
founder effect
History
range expansion
Founder Effect
coalescence
homogenization
ecologists
Postglacial
Gene Flow
gene flow
population structure

Bibliographical note

© 2019 John Wiley & Sons Ltd.

Keywords

  • Admixture
  • Drift
  • Genomics
  • Population structure
  • Secondary contact

Cite this

Foote, A. D., Martin, M. D., Louis, M., Pacheco, G., Robertson, K. M., Sinding, M-H. S., ... Morin, P. A. (2019). Killer whale genomes reveal a complex history of recurrent admixture and vicariance. Molecular Ecology, 28(14), 3427-3444. https://doi.org/10.1111/mec.15099
Foote, Andrew D ; Martin, Michael D ; Louis, Marie ; Pacheco, George ; Robertson, Kelly M ; Sinding, Mikkel-Holger S ; Amaral, Ana R ; Baird, Robin W ; Baker, Charles Scott ; Ballance, Lisa ; Barlow, Jay ; Brownlow, Andrew ; Collins, Tim ; Constantine, Rochelle ; Dabin, Willy ; Dalla Rosa, Luciano ; Davison, Nicholas J ; Durban, John W ; Esteban, Ruth ; Ferguson, Steven H ; Gerrodette, Tim ; Guinet, Christophe ; Hanson, M Bradley ; Hoggard, Wayne ; Matthews, Cory J D ; Samarra, Filipa I P ; de Stephanis, Renaud ; Tavares, Sara B ; Tixier, Paul ; Totterdell, John A ; Wade, Paul ; Excoffier, Laurent ; Gilbert, M Thomas P ; Wolf, Jochen B W ; Morin, Phillip A. / Killer whale genomes reveal a complex history of recurrent admixture and vicariance. In: Molecular Ecology. 2019 ; Vol. 28, No. 14. pp. 3427-3444.
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Foote, AD, Martin, MD, Louis, M, Pacheco, G, Robertson, KM, Sinding, M-HS, Amaral, AR, Baird, RW, Baker, CS, Ballance, L, Barlow, J, Brownlow, A, Collins, T, Constantine, R, Dabin, W, Dalla Rosa, L, Davison, NJ, Durban, JW, Esteban, R, Ferguson, SH, Gerrodette, T, Guinet, C, Hanson, MB, Hoggard, W, Matthews, CJD, Samarra, FIP, de Stephanis, R, Tavares, SB, Tixier, P, Totterdell, JA, Wade, P, Excoffier, L, Gilbert, MTP, Wolf, JBW & Morin, PA 2019, 'Killer whale genomes reveal a complex history of recurrent admixture and vicariance', Molecular Ecology, vol. 28, no. 14, pp. 3427-3444. https://doi.org/10.1111/mec.15099

Killer whale genomes reveal a complex history of recurrent admixture and vicariance. / Foote, Andrew D; Martin, Michael D; Louis, Marie; Pacheco, George; Robertson, Kelly M; Sinding, Mikkel-Holger S; Amaral, Ana R; Baird, Robin W; Baker, Charles Scott; Ballance, Lisa; Barlow, Jay; Brownlow, Andrew; Collins, Tim; Constantine, Rochelle; Dabin, Willy; Dalla Rosa, Luciano; Davison, Nicholas J; Durban, John W; Esteban, Ruth; Ferguson, Steven H; Gerrodette, Tim; Guinet, Christophe; Hanson, M Bradley; Hoggard, Wayne; Matthews, Cory J D; Samarra, Filipa I P; de Stephanis, Renaud; Tavares, Sara B; Tixier, Paul; Totterdell, John A; Wade, Paul; Excoffier, Laurent; Gilbert, M Thomas P; Wolf, Jochen B W; Morin, Phillip A.

In: Molecular Ecology, Vol. 28, No. 14, 07.2019, p. 3427-3444.

Research output: Contribution to journalArticle

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AU - Baker, Charles Scott

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AU - Barlow, Jay

AU - Brownlow, Andrew

AU - Collins, Tim

AU - Constantine, Rochelle

AU - Dabin, Willy

AU - Dalla Rosa, Luciano

AU - Davison, Nicholas J

AU - Durban, John W

AU - Esteban, Ruth

AU - Ferguson, Steven H

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AU - Guinet, Christophe

AU - Hanson, M Bradley

AU - Hoggard, Wayne

AU - Matthews, Cory J D

AU - Samarra, Filipa I P

AU - de Stephanis, Renaud

AU - Tavares, Sara B

AU - Tixier, Paul

AU - Totterdell, John A

AU - Wade, Paul

AU - Excoffier, Laurent

AU - Gilbert, M Thomas P

AU - Wolf, Jochen B W

AU - Morin, Phillip A

N1 - © 2019 John Wiley & Sons Ltd.

PY - 2019/7

Y1 - 2019/7

N2 - Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

AB - Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

KW - Admixture

KW - Drift

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KW - Secondary contact

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Foote AD, Martin MD, Louis M, Pacheco G, Robertson KM, Sinding M-HS et al. Killer whale genomes reveal a complex history of recurrent admixture and vicariance. Molecular Ecology. 2019 Jul;28(14):3427-3444. https://doi.org/10.1111/mec.15099