Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina

Abstract Transgenerational plasticity (TGP)—when a parent or previous generation's environmental experience affects offspring phenotype without involving a genetic change—can be an important mechanism allowing for rapid adaptation. However, despite increasing numbers of empirical examples of TG...

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Main Authors: Isabelle P. Neylan, Andrew Sih, John J. Stachowicz
Format: Article
Language:English
Published: Wiley 2022-11-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.9524
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author Isabelle P. Neylan
Andrew Sih
John J. Stachowicz
author_facet Isabelle P. Neylan
Andrew Sih
John J. Stachowicz
author_sort Isabelle P. Neylan
collection DOAJ
description Abstract Transgenerational plasticity (TGP)—when a parent or previous generation's environmental experience affects offspring phenotype without involving a genetic change—can be an important mechanism allowing for rapid adaptation. However, despite increasing numbers of empirical examples of TGP, there appears to be considerable variation in its strength and direction, yet limited understanding of what causes this variation. We compared patterns of TGP in response to stress across two populations with high versus low historical levels of stress exposure. Specifically, we expected that exposure to acute stress in the population experiencing historically high levels of stress would result in adaptive TGP or alternatively fixed tolerance (no parental effect), whereas the population with low levels of historical exposure would result in negative parental carryover effects. Using a common sessile marine invertebrate, Bugula neritina, and a split brood design, we exposed parents from both populations to copper or control treatments in the laboratory and then had them brood copper‐naïve larvae. We then exposed half of each larval brood to copper and half to control conditions before allowing them to grow to maturity in the field. Maternal copper exposure had a strong negative carryover effect on adult offspring growth and survival in the population without historical exposure, especially when larvae themselves were exposed to copper. We found little to no maternal or offspring treatment effect on adult growth and survival in the population with a history of copper exposure. However, parents from this population produced larger larvae on average and were able to increase the size of their larvae in response to copper exposure, providing a potential mechanism for maintaining fitness and suggesting TGP through maternal provisioning. These results indicate that the ability to adjust offspring phenotype via TGP may be a locally adapted trait and potentially influenced by past patterns of exposure.
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spelling doaj.art-47fdf333248743abacbeff6f2b3c88702022-12-22T02:55:28ZengWileyEcology and Evolution2045-77582022-11-011211n/an/a10.1002/ece3.9524Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritinaIsabelle P. Neylan0Andrew Sih1John J. Stachowicz2Department of Evolution & Ecology, Center for Population Biology UC Davis Davis CA USADepartment of Environmental Science & Policy UC Davis Davis CA USADepartment of Evolution & Ecology, Center for Population Biology UC Davis Davis CA USAAbstract Transgenerational plasticity (TGP)—when a parent or previous generation's environmental experience affects offspring phenotype without involving a genetic change—can be an important mechanism allowing for rapid adaptation. However, despite increasing numbers of empirical examples of TGP, there appears to be considerable variation in its strength and direction, yet limited understanding of what causes this variation. We compared patterns of TGP in response to stress across two populations with high versus low historical levels of stress exposure. Specifically, we expected that exposure to acute stress in the population experiencing historically high levels of stress would result in adaptive TGP or alternatively fixed tolerance (no parental effect), whereas the population with low levels of historical exposure would result in negative parental carryover effects. Using a common sessile marine invertebrate, Bugula neritina, and a split brood design, we exposed parents from both populations to copper or control treatments in the laboratory and then had them brood copper‐naïve larvae. We then exposed half of each larval brood to copper and half to control conditions before allowing them to grow to maturity in the field. Maternal copper exposure had a strong negative carryover effect on adult offspring growth and survival in the population without historical exposure, especially when larvae themselves were exposed to copper. We found little to no maternal or offspring treatment effect on adult growth and survival in the population with a history of copper exposure. However, parents from this population produced larger larvae on average and were able to increase the size of their larvae in response to copper exposure, providing a potential mechanism for maintaining fitness and suggesting TGP through maternal provisioning. These results indicate that the ability to adjust offspring phenotype via TGP may be a locally adapted trait and potentially influenced by past patterns of exposure.https://doi.org/10.1002/ece3.9524bryozoanBugula neritinacopperlocal adaptationtransgenerational plasticity
spellingShingle Isabelle P. Neylan
Andrew Sih
John J. Stachowicz
Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
Ecology and Evolution
bryozoan
Bugula neritina
copper
local adaptation
transgenerational plasticity
title Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
title_full Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
title_fullStr Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
title_full_unstemmed Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
title_short Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina
title_sort local adaptation in the transgenerational response to copper pollution in the bryozoan bugula neritina
topic bryozoan
Bugula neritina
copper
local adaptation
transgenerational plasticity
url https://doi.org/10.1002/ece3.9524
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