Local adaptation with gene flow in a highly dispersive shark

Abstract Adaptive divergence in response to environmental clines are expected to be common in species occupying heterogeneous environments. Despite numerous advances in techniques appropriate for non‐model species, gene–environment association studies in elasmobranchs are still scarce. The bronze wh...

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Main Authors: Juliana D. Klein, Simo N. Maduna, Matthew L. Dicken, Charlene daSilva, Michelle Soekoe, Meaghen E. McCord, Warren M. Potts, Snorre B. Hagen, Aletta E. Bester‐van der Merwe
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13628
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author Juliana D. Klein
Simo N. Maduna
Matthew L. Dicken
Charlene daSilva
Michelle Soekoe
Meaghen E. McCord
Warren M. Potts
Snorre B. Hagen
Aletta E. Bester‐van der Merwe
author_facet Juliana D. Klein
Simo N. Maduna
Matthew L. Dicken
Charlene daSilva
Michelle Soekoe
Meaghen E. McCord
Warren M. Potts
Snorre B. Hagen
Aletta E. Bester‐van der Merwe
author_sort Juliana D. Klein
collection DOAJ
description Abstract Adaptive divergence in response to environmental clines are expected to be common in species occupying heterogeneous environments. Despite numerous advances in techniques appropriate for non‐model species, gene–environment association studies in elasmobranchs are still scarce. The bronze whaler or copper shark (Carcharhinus brachyurus) is a large coastal shark with a wide distribution and one of the most exploited elasmobranchs in southern Africa. Here, we assessed the distribution of neutral and adaptive genomic diversity in C. brachyurus across a highly heterogeneous environment in southern Africa based on genome‐wide SNPs obtained through a restriction site‐associated DNA method (3RAD). A combination of differentiation‐based genome‐scan (outflank) and genotype–environment analyses (redundancy analysis, latent factor mixed models) identified a total of 234 differentiation‐based outlier and candidate SNPs associated with bioclimatic variables. Analysis of 26,299 putatively neutral SNPs revealed moderate and evenly distributed levels of genomic diversity across sites from the east coast of South Africa to Angola. Multivariate and clustering analyses demonstrated a high degree of gene flow with no significant population structuring among or within ocean basins. In contrast, the putatively adaptive SNPs demonstrated the presence of two clusters and deep divergence between Angola and all other individuals from Namibia and South Africa. These results provide evidence for adaptive divergence in response to a heterogeneous seascape in a large, mobile shark despite high levels of gene flow. These results are expected to inform management strategies and policy at the national and regional level for conservation of C. brachyurus populations.
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spelling doaj.art-23ca8294b8c745b78c0c2b164c170f8f2024-02-02T04:15:45ZengWileyEvolutionary Applications1752-45712024-01-01171n/an/a10.1111/eva.13628Local adaptation with gene flow in a highly dispersive sharkJuliana D. Klein0Simo N. Maduna1Matthew L. Dicken2Charlene daSilva3Michelle Soekoe4Meaghen E. McCord5Warren M. Potts6Snorre B. Hagen7Aletta E. Bester‐van der Merwe8Molecular Breeding and Biodiversity Research Group, Department of Genetics Stellenbosch University Stellenbosch South AfricaDepartment of Ecosystems in the Barents Region, Svanhovd Research Station Norwegian Institute of Bioeconomy Research—NIBIO Svanvik NorwayKwaZulu‐Natal Sharks Board Umhlanga Rocks South AfricaDepartment of Forestry, Fisheries and Environment Rogge Bay South AfricaDivision of Marine Science Reel Science Coalition Cape Town South AfricaSouth African Shark Conservancy Hermanus South AfricaDepartment of Ichthyology and Fisheries Science Rhodes University Makhanda South AfricaDepartment of Ecosystems in the Barents Region, Svanhovd Research Station Norwegian Institute of Bioeconomy Research—NIBIO Svanvik NorwayMolecular Breeding and Biodiversity Research Group, Department of Genetics Stellenbosch University Stellenbosch South AfricaAbstract Adaptive divergence in response to environmental clines are expected to be common in species occupying heterogeneous environments. Despite numerous advances in techniques appropriate for non‐model species, gene–environment association studies in elasmobranchs are still scarce. The bronze whaler or copper shark (Carcharhinus brachyurus) is a large coastal shark with a wide distribution and one of the most exploited elasmobranchs in southern Africa. Here, we assessed the distribution of neutral and adaptive genomic diversity in C. brachyurus across a highly heterogeneous environment in southern Africa based on genome‐wide SNPs obtained through a restriction site‐associated DNA method (3RAD). A combination of differentiation‐based genome‐scan (outflank) and genotype–environment analyses (redundancy analysis, latent factor mixed models) identified a total of 234 differentiation‐based outlier and candidate SNPs associated with bioclimatic variables. Analysis of 26,299 putatively neutral SNPs revealed moderate and evenly distributed levels of genomic diversity across sites from the east coast of South Africa to Angola. Multivariate and clustering analyses demonstrated a high degree of gene flow with no significant population structuring among or within ocean basins. In contrast, the putatively adaptive SNPs demonstrated the presence of two clusters and deep divergence between Angola and all other individuals from Namibia and South Africa. These results provide evidence for adaptive divergence in response to a heterogeneous seascape in a large, mobile shark despite high levels of gene flow. These results are expected to inform management strategies and policy at the national and regional level for conservation of C. brachyurus populations.https://doi.org/10.1111/eva.13628adaptive divergenceelasmobranchsgenotype–environment associationpopulation genomicsseascape genomics
spellingShingle Juliana D. Klein
Simo N. Maduna
Matthew L. Dicken
Charlene daSilva
Michelle Soekoe
Meaghen E. McCord
Warren M. Potts
Snorre B. Hagen
Aletta E. Bester‐van der Merwe
Local adaptation with gene flow in a highly dispersive shark
Evolutionary Applications
adaptive divergence
elasmobranchs
genotype–environment association
population genomics
seascape genomics
title Local adaptation with gene flow in a highly dispersive shark
title_full Local adaptation with gene flow in a highly dispersive shark
title_fullStr Local adaptation with gene flow in a highly dispersive shark
title_full_unstemmed Local adaptation with gene flow in a highly dispersive shark
title_short Local adaptation with gene flow in a highly dispersive shark
title_sort local adaptation with gene flow in a highly dispersive shark
topic adaptive divergence
elasmobranchs
genotype–environment association
population genomics
seascape genomics
url https://doi.org/10.1111/eva.13628
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