On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system

Chris J. Brauer, Peter J. Unmack, Steve Smith, Louis Bernatchez, Luciano B. Beheregaray

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high-quality SNP loci and integrated these with models of network connectivity and high-resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.

Original languageEnglish
Pages (from-to)3484-3497
Number of pages14
JournalMolecular Ecology
Volume27
Issue number17
DOIs
Publication statusPublished - 1 Sep 2018

Fingerprint

Metagenomics
Gene Flow
genomics
gene flow
connectivity
Genetic Selection
seasonal variation
Genomics
Rivers
genetic variation
loci
Single Nucleotide Polymorphism
waterways
adaptive radiation
local adaptation
landscape structure
conservation management
species complex
stream flow
natural selection

Cite this

Brauer, Chris J. ; Unmack, Peter J. ; Smith, Steve ; Bernatchez, Louis ; Beheregaray, Luciano B. / On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system. In: Molecular Ecology. 2018 ; Vol. 27, No. 17. pp. 3484-3497.
@article{e2aca3d06c154ad8a153c06c413b69ba,
title = "On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system",
abstract = "Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high-quality SNP loci and integrated these with models of network connectivity and high-resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.",
keywords = "climate change, ddRAD-seq, dendritic networks, landscape genomics, Melanotaenia fluviatilis, Murray-Darling Basin",
author = "Brauer, {Chris J.} and Unmack, {Peter J.} and Steve Smith and Louis Bernatchez and Beheregaray, {Luciano B.}",
year = "2018",
month = "9",
day = "1",
doi = "10.1111/mec.14808",
language = "English",
volume = "27",
pages = "3484--3497",
journal = "Molecular Biology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "17",

}

On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system. / Brauer, Chris J.; Unmack, Peter J.; Smith, Steve; Bernatchez, Louis; Beheregaray, Luciano B.

In: Molecular Ecology, Vol. 27, No. 17, 01.09.2018, p. 3484-3497.

Research output: Contribution to journalArticle

TY - JOUR

T1 - On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system

AU - Brauer, Chris J.

AU - Unmack, Peter J.

AU - Smith, Steve

AU - Bernatchez, Louis

AU - Beheregaray, Luciano B.

PY - 2018/9/1

Y1 - 2018/9/1

N2 - Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high-quality SNP loci and integrated these with models of network connectivity and high-resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.

AB - Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high-quality SNP loci and integrated these with models of network connectivity and high-resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.

KW - climate change

KW - ddRAD-seq

KW - dendritic networks

KW - landscape genomics

KW - Melanotaenia fluviatilis

KW - Murray-Darling Basin

UR - http://www.scopus.com/inward/record.url?scp=85052232156&partnerID=8YFLogxK

U2 - 10.1111/mec.14808

DO - 10.1111/mec.14808

M3 - Article

VL - 27

SP - 3484

EP - 3497

JO - Molecular Biology

JF - Molecular Biology

SN - 0962-1083

IS - 17

ER -