DNA Methylation Carries Signatures of Sublethal Effects Under Thermal Stress in Loggerhead Sea Turtles

IF 3.5 2区 生物学 Q1 EVOLUTIONARY BIOLOGY
Eugenie C. Yen, James D. Gilbert, Alice Balard, Inês O. Afonso, Kirsten Fairweather, Débora Newlands, Artur Lopes, Sandra M. Correia, Albert Taxonera, Stephen J. Rossiter, José M. Martín-Durán, Christophe Eizaguirre
{"title":"DNA Methylation Carries Signatures of Sublethal Effects Under Thermal Stress in Loggerhead Sea Turtles","authors":"Eugenie C. Yen,&nbsp;James D. Gilbert,&nbsp;Alice Balard,&nbsp;Inês O. Afonso,&nbsp;Kirsten Fairweather,&nbsp;Débora Newlands,&nbsp;Artur Lopes,&nbsp;Sandra M. Correia,&nbsp;Albert Taxonera,&nbsp;Stephen J. Rossiter,&nbsp;José M. Martín-Durán,&nbsp;Christophe Eizaguirre","doi":"10.1111/eva.70013","DOIUrl":null,"url":null,"abstract":"<p>To date, studies of the impacts of climate warming on individuals and populations have mostly focused on mortality and thermal tolerance. In contrast, much less is known about the consequences of sublethal effects, which are more challenging to detect, particularly in wild species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch field experiment, we relocated clutches of wild, nesting loggerhead sea turtles (<i>Caretta caretta</i>) to an in situ hatchery. Eggs were then split into two sub-clutches and incubated under shallow or deep conditions, with those in the shallow treatment experiencing significantly higher temperatures in otherwise natural conditions. Although no difference in hatching success was observed between treatments, hatchlings from the shallow, warmer treatment had different length–mass relationships and were weaker at locomotion tests than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. We identified 287 differentially methylated sites between hatchlings from different treatments, including on genes with neurodevelopmental, cytoskeletal, and lipid metabolism functions. Taken together, our results show that higher incubation temperatures induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. These sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming reduces hatchling fitness, which has implications for dispersal capacity and ultimately a population's adaptive potential. Conservation efforts for these endangered species and similar climate-threatened taxa will therefore benefit from strategies for monitoring and mitigating exposure to temperatures that induce sublethal effects.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":null,"pages":null},"PeriodicalIF":3.5000,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70013","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Evolutionary Applications","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/eva.70013","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"EVOLUTIONARY BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

To date, studies of the impacts of climate warming on individuals and populations have mostly focused on mortality and thermal tolerance. In contrast, much less is known about the consequences of sublethal effects, which are more challenging to detect, particularly in wild species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch field experiment, we relocated clutches of wild, nesting loggerhead sea turtles (Caretta caretta) to an in situ hatchery. Eggs were then split into two sub-clutches and incubated under shallow or deep conditions, with those in the shallow treatment experiencing significantly higher temperatures in otherwise natural conditions. Although no difference in hatching success was observed between treatments, hatchlings from the shallow, warmer treatment had different length–mass relationships and were weaker at locomotion tests than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. We identified 287 differentially methylated sites between hatchlings from different treatments, including on genes with neurodevelopmental, cytoskeletal, and lipid metabolism functions. Taken together, our results show that higher incubation temperatures induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. These sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming reduces hatchling fitness, which has implications for dispersal capacity and ultimately a population's adaptive potential. Conservation efforts for these endangered species and similar climate-threatened taxa will therefore benefit from strategies for monitoring and mitigating exposure to temperatures that induce sublethal effects.

Abstract Image

蠵海龟在热应力下的 DNA 甲基化带有亚致死效应的特征
迄今为止,有关气候变暖对个体和种群影响的研究主要集中在死亡率和热耐受性方面。相比之下,人们对亚致死效应后果的了解要少得多,因为亚致死效应的检测更具挑战性,尤其是在生活史隐秘的野生物种中。这就需要开发分子工具来确定其特征。在一个分窝野外实验中,我们将野生筑巢蠵海龟(Caretta caretta)的窝迁移到一个原地孵化场。然后将海龟卵分成两个子群,分别在浅水和深水条件下孵化,其中浅水条件下的海龟卵在其他自然条件下的孵化温度明显更高。虽然在不同的孵化条件下孵化成功率没有差异,但与在温度较低的深层孵化条件下孵化的幼体相比,在温度较高的浅层孵化条件下孵化的幼体具有不同的体长-质量关系,并且在运动测试中表现较弱。为了描述这些热效应的分子特征,我们对孵化时采集的血液样本进行了全基因组亚硫酸氢盐测序。我们在不同处理的幼体之间发现了 287 个不同的甲基化位点,其中包括具有神经发育、细胞骨架和脂质代谢功能的基因。综上所述,我们的研究结果表明,较高的孵化温度会对幼体产生亚致死效应,这反映在其DNA甲基化状态的已识别位点上。这些位点可用作热应激的生物标志物,尤其是当它们在整个生命阶段都保留下来时。总之,这项研究表明,全球变暖会降低幼体的适应能力,从而影响其扩散能力,并最终影响种群的适应潜力。因此,针对这些濒危物种和类似的受气候威胁类群的保护工作将受益于监测和减轻暴露于导致亚致死效应的温度的策略。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Evolutionary Applications
Evolutionary Applications 生物-进化生物学
CiteScore
8.50
自引率
7.30%
发文量
175
审稿时长
6 months
期刊介绍: Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信