Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses

Abstract Comparing the responses of closely related species to environmental changes is an efficient method to explore adaptive divergence, for a better understanding of the adaptive evolution of marine species under rapidly changing climates. Oysters are keystone species thrive in intertidal and es...

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Main Authors: Ziyan Zhang, Ao Li, Zhicai She, Xuegang Wang, Zhen Jia, Wei Wang, Guofan Zhang, Li Li
Format: Article
Language:English
Published: Wiley 2023-02-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13370
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author Ziyan Zhang
Ao Li
Zhicai She
Xuegang Wang
Zhen Jia
Wei Wang
Guofan Zhang
Li Li
author_facet Ziyan Zhang
Ao Li
Zhicai She
Xuegang Wang
Zhen Jia
Wei Wang
Guofan Zhang
Li Li
author_sort Ziyan Zhang
collection DOAJ
description Abstract Comparing the responses of closely related species to environmental changes is an efficient method to explore adaptive divergence, for a better understanding of the adaptive evolution of marine species under rapidly changing climates. Oysters are keystone species thrive in intertidal and estuarine areas where frequent environmental disturbance occurs including fluctuant salinity. The evolutionary divergence of two sister species of sympatric estuarine oysters, Crassostrea hongkongensis and Crassostrea ariakensis, in response to euryhaline habitats on phenotypes and gene expression, and the relative contribution of species effect, environment effect, and their interaction to the divergence were explored. After a 2‐month outplanting at high‐ and low‐salinity locations in the same estuary, the high growth rate, percent survival, and high tolerance indicated by physiological parameters suggested that the fitness of C. ariakensis was higher under high‐salinity conditions and that of C. hongkongensis was higher under low‐salinity conditions. Moreover, a transcriptomic analysis showed the two species exhibited differentiated transcriptional expression in high‐ and low‐salinity habitats, largely caused by the species effect. Several of the important pathways enriched in divergent genes between species were also salinity‐responsive pathways. Specifically, the pyruvate and taurine metabolism pathway and several solute carriers may contribute to the hyperosmotic adaptation of C. ariakensis, and some solute carriers may contribute to the hypoosmotic adaptation of C. hongkongensis. Our findings provide insights into the phenotypic and molecular mechanisms underlying salinity adaptation in marine mollusks, which will facilitate the assessment of the adaptive capacity of marine species in the context of climate change and will also provide practical information for marine resource conservation and aquaculture.
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spelling doaj.art-aa0a0f667a7347c0be6f379b7cd93b6c2023-02-13T09:56:24ZengWileyEvolutionary Applications1752-45712023-02-0116223424910.1111/eva.13370Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analysesZiyan Zhang0Ao Li1Zhicai She2Xuegang Wang3Zhen Jia4Wei Wang5Guofan Zhang6Li Li7CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaGuangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences Beibu Gulf University Qinzhou ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaGuangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences Beibu Gulf University Qinzhou ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega‐Science, Institute of Oceanology Chinese Academy of Sciences Qingdao ChinaAbstract Comparing the responses of closely related species to environmental changes is an efficient method to explore adaptive divergence, for a better understanding of the adaptive evolution of marine species under rapidly changing climates. Oysters are keystone species thrive in intertidal and estuarine areas where frequent environmental disturbance occurs including fluctuant salinity. The evolutionary divergence of two sister species of sympatric estuarine oysters, Crassostrea hongkongensis and Crassostrea ariakensis, in response to euryhaline habitats on phenotypes and gene expression, and the relative contribution of species effect, environment effect, and their interaction to the divergence were explored. After a 2‐month outplanting at high‐ and low‐salinity locations in the same estuary, the high growth rate, percent survival, and high tolerance indicated by physiological parameters suggested that the fitness of C. ariakensis was higher under high‐salinity conditions and that of C. hongkongensis was higher under low‐salinity conditions. Moreover, a transcriptomic analysis showed the two species exhibited differentiated transcriptional expression in high‐ and low‐salinity habitats, largely caused by the species effect. Several of the important pathways enriched in divergent genes between species were also salinity‐responsive pathways. Specifically, the pyruvate and taurine metabolism pathway and several solute carriers may contribute to the hyperosmotic adaptation of C. ariakensis, and some solute carriers may contribute to the hypoosmotic adaptation of C. hongkongensis. Our findings provide insights into the phenotypic and molecular mechanisms underlying salinity adaptation in marine mollusks, which will facilitate the assessment of the adaptive capacity of marine species in the context of climate change and will also provide practical information for marine resource conservation and aquaculture.https://doi.org/10.1111/eva.13370adaptive divergenceoystersphenotypic and transcriptomic analysesrelated speciessalinity gradient
spellingShingle Ziyan Zhang
Ao Li
Zhicai She
Xuegang Wang
Zhen Jia
Wei Wang
Guofan Zhang
Li Li
Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
Evolutionary Applications
adaptive divergence
oysters
phenotypic and transcriptomic analyses
related species
salinity gradient
title Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
title_full Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
title_fullStr Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
title_full_unstemmed Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
title_short Adaptive divergence and underlying mechanisms in response to salinity gradients between two Crassostrea oysters revealed by phenotypic and transcriptomic analyses
title_sort adaptive divergence and underlying mechanisms in response to salinity gradients between two crassostrea oysters revealed by phenotypic and transcriptomic analyses
topic adaptive divergence
oysters
phenotypic and transcriptomic analyses
related species
salinity gradient
url https://doi.org/10.1111/eva.13370
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