Disentangling structural genomic and behavioural barriers in a sea of connectivity

Julia M.I. Barth; David Villegas-Ríos; Carla Freitas; Even Moland; Bastiaan Star; Carl André; Halvor Knutsen; Ian Bradbury; Jan Dierking; Christoph Petereit; David Righton; Julian Metcalfe; Kjetill S. Jakobsen; Esben M. Olsen; Sissel Jentoft

doi:10.1111/mec.15010

Disentangling structural genomic and behavioural barriers in a sea of connectivity

Julia M.I. Barth, David Villegas-Ríos, Carla Freitas, Even Moland, Bastiaan Star, Carl André, Halvor Knutsen, Ian Bradbury, Jan Dierking, Christoph Petereit, David Righton, Julian Metcalfe, Kjetill S. Jakobsen, Esben M. Olsen, Sissel Jentoft

Producción científica: Contribución a una revista › Artículo › revisión exhaustiva

72 Citas (Scopus)

Resumen

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

Idioma original	English
Páginas (desde-hasta)	1394-1411
Número de páginas	18
Publicación	Molecular Ecology
Volumen	28
N.º	6
DOI	https://doi.org/10.1111/mec.15010
Estado	Published - mar. 2019
Publicado de forma externa	Sí

Nota bibliográfica

Funding Information:
We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/ O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at GD?teborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R.

Funding Information:
We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at Göteborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R.

Funding Information:
Research Council of Norway (RCN) “The Aqua Genome Project”, Grant/Award Number: 221734/O30; RCN “Ecogenome project”, Grant/Award Number: 280453/ E40; Centre for Marine Evolutionary Biology at GD?teborg University; Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, Grant/Award Number: #625852

Publisher Copyright:
© 2019 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd

ASJC Scopus Subject Areas

Ecology, Evolution, Behavior and Systematics
Genetics

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

ODS de las Naciones Unidas

Este resultado contribuye a los siguientes Objetivos de Desarrollo Sostenible

Acceder al documento

10.1111/mec.15010

Otros archivos y enlaces

Citar esto

Barth, J. M. I., Villegas-Ríos, D., Freitas, C., Moland, E., Star, B., André, C., Knutsen, H., Bradbury, I., Dierking, J., Petereit, C., Righton, D., Metcalfe, J., Jakobsen, K. S., Olsen, E. M., & Jentoft, S. (2019). Disentangling structural genomic and behavioural barriers in a sea of connectivity. Molecular Ecology, 28(6), 1394-1411. https://doi.org/10.1111/mec.15010

@article{d31319afffd44412b5e9a4f6dd0bbe66,

title = "Disentangling structural genomic and behavioural barriers in a sea of connectivity",

abstract = "Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.",

author = "Barth, {Julia M.I.} and David Villegas-R{\'i}os and Carla Freitas and Even Moland and Bastiaan Star and Carl Andr{\'e} and Halvor Knutsen and Ian Bradbury and Jan Dierking and Christoph Petereit and David Righton and Julian Metcalfe and Jakobsen, {Kjetill S.} and Olsen, {Esben M.} and Sissel Jentoft",

note = "Funding Information: We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/ O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at GD?teborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R. Funding Information: We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at G{\"o}teborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R. Funding Information: Research Council of Norway (RCN) “The Aqua Genome Project”, Grant/Award Number: 221734/O30; RCN “Ecogenome project”, Grant/Award Number: 280453/ E40; Centre for Marine Evolutionary Biology at GD?teborg University; Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, Grant/Award Number: #625852 Publisher Copyright: {\textcopyright} 2019 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd",

year = "2019",

month = mar,

doi = "10.1111/mec.15010",

language = "English",

volume = "28",

pages = "1394--1411",

journal = "Molecular Ecology",

issn = "0962-1083",

publisher = "Wiley-Blackwell",

number = "6",

}

TY - JOUR

T1 - Disentangling structural genomic and behavioural barriers in a sea of connectivity

AU - Barth, Julia M.I.

AU - Villegas-Ríos, David

AU - Freitas, Carla

AU - Moland, Even

AU - Star, Bastiaan

AU - André, Carl

AU - Knutsen, Halvor

AU - Bradbury, Ian

AU - Dierking, Jan

AU - Petereit, Christoph

AU - Righton, David

AU - Metcalfe, Julian

AU - Jakobsen, Kjetill S.

AU - Olsen, Esben M.

AU - Jentoft, Sissel

N1 - Funding Information: We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/ O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at GD?teborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R. Funding Information: We thank H. T. Baalsrud and M. Matschiner for assistance in sampling, M. Skage, S. Kollias, A. Tooming-Klunderud, M. H. Selander Hansen, and H. Rydbeck from the Norwegian Sequencing Centre for sequencing and processing of samples, and four anonymous reviewers for their constructive comments that greatly improved the manuscript. J.M.I.B. thanks W. Salzburger for providing a stimulating workspace. The computational genomic work was performed on the Abel Cluster, owned by the University of Oslo and the Norwegian metacentre for High Performance Computing (NOTUR), and operated by the Department for Research Computing at the University of Oslo IT-department (USIT). This work was funded by the Research Council of Norway (RCN) through “The Aqua Genome Project” (221734/O30) to K.S.J. Additional support was also obtained by the RCN “Ecogenome project” (280453/E40) to H.K., by the Centre for Marine Evolutionary Biology at Göteborg University to C.A., and a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, project #625852 (BE-FISH) granted to D.V.R. Funding Information: Research Council of Norway (RCN) “The Aqua Genome Project”, Grant/Award Number: 221734/O30; RCN “Ecogenome project”, Grant/Award Number: 280453/ E40; Centre for Marine Evolutionary Biology at GD?teborg University; Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, Grant/Award Number: #625852 Publisher Copyright: © 2019 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd

PY - 2019/3

Y1 - 2019/3

N2 - Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

AB - Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

UR - http://www.scopus.com/inward/record.url?scp=85062973539&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85062973539&partnerID=8YFLogxK

U2 - 10.1111/mec.15010

DO - 10.1111/mec.15010

M3 - Article

C2 - 30633410

AN - SCOPUS:85062973539

SN - 0962-1083

VL - 28

SP - 1394

EP - 1411

JO - Molecular Ecology

JF - Molecular Ecology

IS - 6

ER -

Disentangling structural genomic and behavioural barriers in a sea of connectivity

Resumen

Nota bibliográfica

ASJC Scopus Subject Areas

PubMed: MeSH publication types

ODS de las Naciones Unidas

Acceder al documento

Otros archivos y enlaces

Huella

Citar esto