Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer

Abstract Rising ocean temperatures and extreme temperature events have precipitated declines and local extinctions in many marine species globally, but patterns of loss are often uneven across species ranges for reasons that are poorly understood. Knowledge of the extent of local adaptation and gene...

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Main Authors: Adam D. Miller, Melinda A. Coleman, Jennifer Clark, Rachael Cook, Zuraya Naga, Martina A. Doblin, Ary A. Hoffmann, Craig D. H. Sherman, Alecia Bellgrove
Format: Article
Language:English
Published: Wiley 2020-05-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12909
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author Adam D. Miller
Melinda A. Coleman
Jennifer Clark
Rachael Cook
Zuraya Naga
Martina A. Doblin
Ary A. Hoffmann
Craig D. H. Sherman
Alecia Bellgrove
author_facet Adam D. Miller
Melinda A. Coleman
Jennifer Clark
Rachael Cook
Zuraya Naga
Martina A. Doblin
Ary A. Hoffmann
Craig D. H. Sherman
Alecia Bellgrove
author_sort Adam D. Miller
collection DOAJ
description Abstract Rising ocean temperatures and extreme temperature events have precipitated declines and local extinctions in many marine species globally, but patterns of loss are often uneven across species ranges for reasons that are poorly understood. Knowledge of the extent of local adaptation and gene flow may explain such patterns and help predict future trajectories under scenarios of climate change. We test the extent to which local differentiation in thermal tolerance is influenced by gene flow and local adaptation using a widely distributed intertidal seaweed (Hormosira banksii) from temperate Australia. Population surveys across ~2,000 km of the species range revealed strong genetic structuring at regional and local scales (global FST = 0.243) reflecting extremely limited gene flow, while common garden experiments (14‐day exposures to 15, 18, 21°C) revealed strong site differences in early development and mortality in response to elevated temperature. Embryos from many sites spanning a longitudinal thermal gradient showed suppressed development and increased mortality to elevated water temperatures, but populations originating from warmer and more variable thermal environments tended to be less susceptible to warming. Notably, there was significant local‐scale variation in the thermal responses of embryos within regions which was corroborated by the finding of small‐scale genetic differences. We expect the observed genetic and phenotypic differentiation to lead to uneven responses to warming sea surface temperatures in this important marine foundation species. The study highlights the challenges of predicting species responses to thermal stress and the importance of management strategies that incorporate evolutionary potential for “climate‐proofing” marine ecosystems.
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spelling doaj.art-5bfad97fe3794f3cb5654390e001116e2022-12-22T02:49:22ZengWileyEvolutionary Applications1752-45712020-05-0113591893410.1111/eva.12909Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineerAdam D. Miller0Melinda A. Coleman1Jennifer Clark2Rachael Cook3Zuraya Naga4Martina A. Doblin5Ary A. Hoffmann6Craig D. H. Sherman7Alecia Bellgrove8School of Life and Environmental Sciences Centre for Integrative Ecology Deakin University Geelong Vic. AustraliaNSW Fisheries National Marine Science Centre Coffs Harbour NSW AustraliaClimate Change Cluster University of Technology Sydney Sydney NSW AustraliaSchool of Life and Environmental Sciences Centre for Integrative Ecology Deakin University Geelong Vic. AustraliaSchool of Life and Environmental Sciences Centre for Integrative Ecology Deakin University Geelong Vic. AustraliaDepartment of Botany University of British Columbia Vancouver BC CanadaSchool of BioSciences Bio21 Institute The University of Melbourne Parkville Vic. AustraliaSchool of Life and Environmental Sciences Centre for Integrative Ecology Deakin University Geelong Vic. AustraliaSchool of Life and Environmental Sciences Centre for Integrative Ecology Deakin University Geelong Vic. AustraliaAbstract Rising ocean temperatures and extreme temperature events have precipitated declines and local extinctions in many marine species globally, but patterns of loss are often uneven across species ranges for reasons that are poorly understood. Knowledge of the extent of local adaptation and gene flow may explain such patterns and help predict future trajectories under scenarios of climate change. We test the extent to which local differentiation in thermal tolerance is influenced by gene flow and local adaptation using a widely distributed intertidal seaweed (Hormosira banksii) from temperate Australia. Population surveys across ~2,000 km of the species range revealed strong genetic structuring at regional and local scales (global FST = 0.243) reflecting extremely limited gene flow, while common garden experiments (14‐day exposures to 15, 18, 21°C) revealed strong site differences in early development and mortality in response to elevated temperature. Embryos from many sites spanning a longitudinal thermal gradient showed suppressed development and increased mortality to elevated water temperatures, but populations originating from warmer and more variable thermal environments tended to be less susceptible to warming. Notably, there was significant local‐scale variation in the thermal responses of embryos within regions which was corroborated by the finding of small‐scale genetic differences. We expect the observed genetic and phenotypic differentiation to lead to uneven responses to warming sea surface temperatures in this important marine foundation species. The study highlights the challenges of predicting species responses to thermal stress and the importance of management strategies that incorporate evolutionary potential for “climate‐proofing” marine ecosystems.https://doi.org/10.1111/eva.12909climate changeevolutionary potentialgene flowlocal adaptationmarine ecosystem engineer
spellingShingle Adam D. Miller
Melinda A. Coleman
Jennifer Clark
Rachael Cook
Zuraya Naga
Martina A. Doblin
Ary A. Hoffmann
Craig D. H. Sherman
Alecia Bellgrove
Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
Evolutionary Applications
climate change
evolutionary potential
gene flow
local adaptation
marine ecosystem engineer
title Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
title_full Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
title_fullStr Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
title_full_unstemmed Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
title_short Local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
title_sort local thermal adaptation and limited gene flow constrain future climate responses of a marine ecosystem engineer
topic climate change
evolutionary potential
gene flow
local adaptation
marine ecosystem engineer
url https://doi.org/10.1111/eva.12909
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