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. Ferguson; Tim 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

doi:10.1111/mec.15099

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

13 Citations (Scopus)

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 language	English
Journal	Molecular Ecology
Volume	28
Issue number	14
Pages (from-to)	3427-3444
Number of pages	18
ISSN	0962-1083
DOIs	https://doi.org/10.1111/mec.15099
Publication status	Published - 2019

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Foote, A. D., Martin, M. D., Louis, M., Pacheco, G., Robertson, K. M., Sinding, M.-H. S., Amaral, A. R., Baird, R. W., Baker, C. S., Ballance, L., Barlow, J., Brownlow, A., Collins, T., Constantine, R., Dabin, W., Dalla Rosa, L., Davison, N. J., Durban, J. W., Esteban, R., ... 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, 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

@article{757880ffaac5479e8d3d3165f994ab6d,

title = "Killer whale genomes reveal a complex history of recurrent admixture and vicariance",

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.",

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

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TY - JOUR

T1 - Killer whale genomes reveal a complex history of recurrent admixture and vicariance

AU - Foote, Andrew D.

AU - Martin, Michael D.

AU - Louis, Marie

AU - Pacheco, George

AU - Robertson, Kelly M

AU - Sinding, Mikkel-Holger S

AU - Amaral, Ana R

AU - Baird, Robin W.

AU - Baker, Charles Scott

AU - Ballance, Lisa

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.

AU - Gerrodette, Tim

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.

PY - 2019

Y1 - 2019

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.

U2 - 10.1111/mec.15099

DO - 10.1111/mec.15099

M3 - Journal article

C2 - 31131963

SN - 0962-1083

VL - 28

SP - 3427

EP - 3444

JO - Molecular Ecology

JF - Molecular Ecology

IS - 14

ER -

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

Abstract

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