Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

Sarah J. Salisbury; Robert Perry; Don Keefe; Gregory R. McCracken; Kara K.S. Layton; Tony Kess; Ian R. Bradbury; Daniel E. Ruzzante

doi:10.1111/mec.16913

Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

Sarah J. Salisbury^*
, Robert Perry
, Don Keefe
, Gregory R. McCracken
, Kara K.S. Layton
, Tony Kess
, Ian R. Bradbury
, Daniel E. Ruzzante

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

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

8 Citations (Scopus)

3 Downloads (Pure)

Abstract

Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

Original language	English
Pages (from-to)	3025-3043
Number of pages	19
Journal	Molecular Ecology
Volume	32
Issue number	12
Early online date	3 Mar 2023
DOIs	https://doi.org/10.1111/mec.16913
Publication status	Published - Jun 2023

Bibliographical note

Funding Information:
Thanks go to our editor and three anonymous reviewers whose suggestions greatly improved this study. We thank S. Avery, J. Callahan, S. Duffy, S. Hann, L. Pike, R. Solomon, A. Walsh, for assistance with sample collection and fieldwork. We are grateful to X. Dallaire and J.S. Moore for providing samples from Ungava, Bay (HAB) and to L. Bernatchez for his valuable comments on an earlier version of this manuscript. Thanks to Parks Canada for allowing us access to the Torngat Mountains National Park and the Nunatsiavut government for allowing us to collect samples from their lands. Thanks to A. Belay at Mount Sinai Hospital for her help with sequencing, A. Mesmer for help with genotyping, and S. Lehnert for insightful data analysis suggestions. We also thank the Institute for Biodiversity, Ecosystem Science, and Sustainability of the Department of Environment and Conservation of the Government of Labrador and Newfoundland for funding for this project; NSERC for the Strategic Grant STPGP 430198 and Discovery Grant awarded to DER, for the CGS‐D awarded to SJS; the Killam Trust for the Level 2 Izaak awarded to SJS; and the Government of Nova Scotia for the Graduate Scholarship awarded to SJS.

Publisher Copyright:
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Data Availability Statement

A .ped file and corresponding .map file for all samples has been deposited in Dryad and is available at: https://doi.org/10.5061/dryad.wdbrv15sg. Additional metadata including weight, fork length, sex, maturity, and mtDNA D-loop haplotype (as assigned by Salisbury et al., 2019) measured for samples collected between 2010 and 2015 are available in Supporting Information Appendix S2

Funding

Thanks go to our editor and three anonymous reviewers whose suggestions greatly improved this study. We thank S. Avery, J. Callahan, S. Duffy, S. Hann, L. Pike, R. Solomon, A. Walsh, for assistance with sample collection and fieldwork. We are grateful to X. Dallaire and J.S. Moore for providing samples from Ungava, Bay (HAB) and to L. Bernatchez for his valuable comments on an earlier version of this manuscript. Thanks to Parks Canada for allowing us access to the Torngat Mountains National Park and the Nunatsiavut government for allowing us to collect samples from their lands. Thanks to A. Belay at Mount Sinai Hospital for her help with sequencing, A. Mesmer for help with genotyping, and S. Lehnert for insightful data analysis suggestions. We also thank the Institute for Biodiversity, Ecosystem Science, and Sustainability of the Department of Environment and Conservation of the Government of Labrador and Newfoundland for funding for this project; NSERC for the Strategic Grant STPGP 430198 and Discovery Grant awarded to DER, for the CGS‐D awarded to SJS; the Killam Trust for the Level 2 Izaak awarded to SJS; and the Government of Nova Scotia for the Graduate Scholarship awarded to SJS.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 13 Climate Action

Keywords

anadromy
colonization history
gene flow
isolation by distance
local adaptation
morph

Access to Document

10.1111/mec.16913Licence: CC BY-NC

Salisbury_ME_Geography_Enviroment_and_VOR
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. https://creativecommons.org/licenses/by-nc/4.0/ © 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd
Final published version, 4.6 MBLicence: CC BY-NC

Cite this

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title = "Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish",

abstract = "Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.",

keywords = "anadromy, colonization history, gene flow, isolation by distance, local adaptation, morph",

author = "Salisbury, \{Sarah J.\} and Robert Perry and Don Keefe and McCracken, \{Gregory R.\} and Layton, \{Kara K.S.\} and Tony Kess and Bradbury, \{Ian R.\} and Ruzzante, \{Daniel E.\}",

note = "Funding Information: Thanks go to our editor and three anonymous reviewers whose suggestions greatly improved this study. We thank S. Avery, J. Callahan, S. Duffy, S. Hann, L. Pike, R. Solomon, A. Walsh, for assistance with sample collection and fieldwork. We are grateful to X. Dallaire and J.S. Moore for providing samples from Ungava, Bay (HAB) and to L. Bernatchez for his valuable comments on an earlier version of this manuscript. Thanks to Parks Canada for allowing us access to the Torngat Mountains National Park and the Nunatsiavut government for allowing us to collect samples from their lands. Thanks to A. Belay at Mount Sinai Hospital for her help with sequencing, A. Mesmer for help with genotyping, and S. Lehnert for insightful data analysis suggestions. We also thank the Institute for Biodiversity, Ecosystem Science, and Sustainability of the Department of Environment and Conservation of the Government of Labrador and Newfoundland for funding for this project; NSERC for the Strategic Grant STPGP 430198 and Discovery Grant awarded to DER, for the CGS‐D awarded to SJS; the Killam Trust for the Level 2 Izaak awarded to SJS; and the Government of Nova Scotia for the Graduate Scholarship awarded to SJS. Publisher Copyright: {\textcopyright} 2023 The Authors. Molecular Ecology published by John Wiley \& Sons Ltd.",

year = "2023",

month = jun,

doi = "10.1111/mec.16913",

language = "English",

volume = "32",

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journal = "Molecular Ecology",

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T1 - Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

AU - Salisbury, Sarah J.

AU - Perry, Robert

AU - Keefe, Don

AU - McCracken, Gregory R.

AU - Layton, Kara K.S.

AU - Kess, Tony

AU - Bradbury, Ian R.

AU - Ruzzante, Daniel E.

N1 - Funding Information: Thanks go to our editor and three anonymous reviewers whose suggestions greatly improved this study. We thank S. Avery, J. Callahan, S. Duffy, S. Hann, L. Pike, R. Solomon, A. Walsh, for assistance with sample collection and fieldwork. We are grateful to X. Dallaire and J.S. Moore for providing samples from Ungava, Bay (HAB) and to L. Bernatchez for his valuable comments on an earlier version of this manuscript. Thanks to Parks Canada for allowing us access to the Torngat Mountains National Park and the Nunatsiavut government for allowing us to collect samples from their lands. Thanks to A. Belay at Mount Sinai Hospital for her help with sequencing, A. Mesmer for help with genotyping, and S. Lehnert for insightful data analysis suggestions. We also thank the Institute for Biodiversity, Ecosystem Science, and Sustainability of the Department of Environment and Conservation of the Government of Labrador and Newfoundland for funding for this project; NSERC for the Strategic Grant STPGP 430198 and Discovery Grant awarded to DER, for the CGS‐D awarded to SJS; the Killam Trust for the Level 2 Izaak awarded to SJS; and the Government of Nova Scotia for the Graduate Scholarship awarded to SJS. Publisher Copyright: © 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

PY - 2023/6

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N2 - Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

AB - Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

KW - anadromy

KW - colonization history

KW - gene flow

KW - isolation by distance

KW - local adaptation

KW - morph

UR - https://www.scopus.com/pages/publications/85152052482

U2 - 10.1111/mec.16913

DO - 10.1111/mec.16913

M3 - Article

AN - SCOPUS:85152052482

SN - 0962-1083

VL - 32

SP - 3025

EP - 3043

JO - Molecular Ecology

JF - Molecular Ecology

IS - 12

ER -

Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

Abstract

Bibliographical note

Data Availability Statement

Funding

UN SDGs

Keywords

Access to Document

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