Meta-analytic data for tolerance plasticity study - literature review from 2019-2020

Website: https://www.bco-dmo.org/dataset/1009144
Data Type: Synthesis
Version: 1
Version Date: 2026-10-06

Project
» Investigating mechanisms underlying adaptive capacity to ocean warming (URO)
ContributorsAffiliationRole
Cheng, BrianUniversity of Massachusetts AmherstPrincipal Investigator
Kelly, MorganLouisiana State University (LSU)Scientist
Mickle, AudreyWoods Hole Oceanographic Institution (WHOI BCO-DMO)BCO-DMO Data Manager

Abstract
Many species face extinction risks owing to climate change, and there is an urgent need to identify which species’ populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism’s upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found fewgeneralizable patterns to explain variation in this trait. Here, we data for a meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. These results advance our understanding of variation in populations’ susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.


Coverage

Location: Global meta-analytic data from published studies. 
Spatial Extent: N:65.4529 E:146.4769 S:-40.65 W:-161.58333
Temporal Extent: 1998-01-01 - 2019-12-31

Methods & Sampling

Studies which measure thermal tolerance plasticity typically collect organisms from nature and acclimate them to different temperatures for defined periods of time in the lab before measuring thermal tolerance. Important methodological considerations for these types of studies include (1) for how long and at what temperature organisms are acclimated, (2) how fast the temperature is changed, and (3) whether measurements are made on field collected or F1 individuals, given that parental conditions are known to influence thermal plasticity. To identify publications for use in our study, we followed PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) guidelines (supplemental figure S1 in Barley et al. 2021). We searched titles, abstracts, and key words in Web of Science (Clarivate Analytics, Philadelphia, USA) using the following search string: (Thermal OR temperatures) AND (Lethal OR “Thermal tolerance” OR “Thermal limit” OR CTmax OR CTmin OR LT50 OR “freezing tolerance”) AND ("Local* Adapt*" OR "“Latitud* Var” OR Intraspecific). We conducted an initial literature search on 24 August 2019 and updated the search on 28 July 2020. We also added studies that we were aware of but were not returned in the literature search. We used the following criteria for inclusion, where each study must have: (1) reported new results of whole-organism upper thermal limit in degrees Celsius for at least 2 populations of the same species, (2) experimentally measured thermal tolerance after acclimating all individuals to at least two temperatures, (3) reported a measure of error for the thermal tolerance estimate, and (4) not measured tolerance of introduced species, hybrid lines, cultivars, domesticated species, or later generations of experimental laboratory populations (greater than F2). Although we initially included both cold and heat tolerance studies, we later excluded cold tolerance studies from our analysis due to insufficient data. Studies of cold tolerance, and additional studies that met criteria (1) and (2) but were excluded based on (3) and/or (4) are listed in supplemental table S1 in Barley et al. 2021. We screened 400 publications that measured thermal tolerances across populations and identified 20 studies to include in our meta-analysis, representing 19 species. The studies that were accepted after looking through titles and abstracts but were later excluded from our analysis are listed in Table S1 in Barley et al. 2021. We extracted data from each publication using relevant figures, tables, text, or supplementary material. In the case of figures, we used WebPlotDigitizer (version 4.3; Rohatgi 2020) to extract means and error estimates.


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Methods
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Methods
Zhao, L., Zhang, Q.-G., & Zhang, D.-Y. (2015). Evolution alters ecological mechanisms of coexistence in experimental microcosms. Functional Ecology, 30(8), 1440–1446. Portico. https://doi.org/10.1111/1365-2435.12611
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Methods
van Heerwaarden, B., Kellermann, V., & Sgrò, C. M. (2016). Limited scope for plasticity to increase upper thermal limits. Functional Ecology, 30(12), 1947–1956. Portico. https://doi.org/10.1111/1365-2435.12687
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Parameters

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Project Information

Investigating mechanisms underlying adaptive capacity to ocean warming (URO)

Coverage: Coastal marine waters of western Atlantic ocean from 31 to 44 degrees latitude N


NSF Award Abstract:
Understanding how marine life copes with drastically different environmental conditions now and into the future is essential for the management and conservation of biodiversity in the ocean. One complicating factor is the observation that populations within a given species are often fine-tuned to the environment that they live in. Yet, it is often unclear what components of the environment create these differences across populations. This project focuses on Atlantic oyster drills, a predatory snail that consumes farmed and wild oysters on the Atlantic coast of North America, the location of one of the strongest temperature gradients in the world. The investigators combine field and laboratory studies to understand how differences in temperature affect the growth and survival of oyster drills sourced from populations throughout their range. This information is paired with molecular analyses to help determine genetic and physiological differences among populations. In addition to benefitting oyster reefs, this information broadly contributes to the understanding of how marine life will respond to rapidly changing environmental conditions. The project also supports the education and marine science training of students at the undergraduate, graduate, and postdoctoral level. In partnership with the non-profit organization Waterstrong, the investigators will provide marine science and swimming skills training to thirty girls from historically underrepresented groups.

Predicting how marine communities will respond to rapid environmental change is difficult because species responses can vary across populations and because organisms may evolve over time. Knowledge of how such evolutionary potential arises and is maintained is limited. A useful approach for examining species response to environmental change is to investigate how species have locally adapted to environmental differences across their range. This project tests competing mechanisms that can generate countergradient variation (CnGV; a widespread form of local adaptation) in an ecologically important marine species (Atlantic oyster drill, Urosalpinx cinerea). The objectives of this integrative research are to 1) quantify the strength of seasonality and mean temperature in generating CnGV and to 2) identify if these responses are correlated across biological traits using a combination of field sampling and common garden experimentation. These objectives are complemented with a molecular approach that 3) quantifies neutral genetic structure across populations and 4) identifies the roles of genetic adaptation and transcriptional plasticity in facilitating physiological adaptation to environmental change. The proposed work is significant because it provides a novel test for different environmental drivers of a commonly observed form of local adaptation. This research also reveals the genetic underpinnings of how such local adaptation arises and will give insight into the adaptive capacity of organisms to rapid change.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

Other project information:
Further information about this project and related work can be found on the UMass Amherst website "MARINE GLOBAL CHANGE ECOLOGY" (http://bscheng.com).



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Funding

Funding SourceAward
NSF Division of Ocean Sciences (NSF OCE)

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