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Greater evolutionary divergence of thermal limits within marine than terrestrial species

Nature Climate Change volume 12, pages 1175–1180 (2022)Cite this article

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Abstract

There is considerable uncertainty regarding which ecosystems are most vulnerable to warming. Current understanding of organismal sensitivity is largely centred on species-level assessments that do not consider variation across populations. Here we used meta-analysis to quantify upper thermal tolerance variation across 305 populations from 61 terrestrial, freshwater, marine and intertidal taxa. We found strong differentiation in heat tolerance across populations in marine and intertidal taxa but not terrestrial or freshwater taxa. This is counter to the expectation that increased connectivity in the ocean should reduce intraspecific variation. Such adaptive differentiation in the ocean suggests there may be standing genetic variation at the species level to buffer climate impacts. Assessments of vulnerability to warming should account for variation in thermal tolerance among populations (or the lack thereof) to improve predictions about climate vulnerability.

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Fig. 1: Conceptual figure outlining hypotheses predicting population-level divergence in thermal limits across realms.
Fig. 2: Population-level patterns in heat tolerance.
Fig. 3: Pairwise heat tolerance comparisons between populations using Hedges’ g. Larger effect sizes indicate greater differentiation in heat tolerance.
Fig. 4: Estimated warming tolerance.

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Data availability

The thermal tolerance data that support the findings of this study are available in a figshare repository78.

Code availability

Custom analysis scripts are available in a figshare repository78.

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Acknowledgements

This article arose from the Research Coordination Network, ‘Evolution in Changing Seas’ (US National Science Foundation #1764316). We thank K. Lotterhos, M. Albecker, D. Bolnick, J. Kelley and G. Trussel for developing and organizing the network. Additional support was provided by the US National Science Foundation (#2023571 to B.S.C.). M.S. was supported by US National Science Foundation grant #1947965. We thank H.G. Dam, E.D. Grosholz and L.M. Komoroske for comments on earlier manuscript drafts. Finally, we are very grateful to the primary authors who collected the empirical data.

Author information

Authors and Affiliations

  1. Department of Marine Sciences, University of Connecticut, Groton, CT, USA

    Matthew Sasaki

  2. Department of Environmental Conservation, University of Massachusetts Amherst, Amherst, MA, USA

    Jordanna M. Barley, Alysha B. Putnam, Andrew R. Villeneuve & Brian S. Cheng

  3. Department of Biological Sciences, University of Massachusetts Lowell, Lowell, MA, USA

    Sarah Gignoux-Wolfsohn

  4. Department of Biology, Keene State College, Keene, NH, USA

    Cynthia G. Hays

  5. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA

    Morgan W. Kelly

  6. Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, USA

    Seema N. Sheth

  7. Department of Biological Sciences, University of New Hampshire, Durham, NH, USA

    Andrew R. Villeneuve

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Contributions

All authors conceptualized and designed the paper. M.S., J.M.B., S.G.-W., C.G.H., M.W.K., A.B.P., S.N.S., A.R.V. and B.S.C. assembled the data; M.S. analysed the data and produced figures. M.S. and B.S.C. drafted the paper; all authors contributed to discussion, writing and interpretation.

Corresponding authors

Correspondence to Matthew Sasaki or Brian S. Cheng.

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Nature Climate Change thanks Richelle Tanner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Flowchart breaking down the number of studies processed during screening, and the number of thermal limits used in our analyses.

A summary of the number of studies processed during screening, the number of thermal limits before and after major filtering, and the number of population pairs and effect size estimates used in our analyses.

Extended Data Fig. 2 Comparison of within- and between-species latitudinal patterns in upper and lower thermal limits.

Comparison of mean intraspecific slope estimates (± SE) for upper and lower thermal tolerance values against latitude for terrestrial taxa (n = 37 lower thermal limit slopes; n = 43 upper thermal limit slopes). Studies examining elevational differences are excluded. For comparison, interspecific slope estimates are included from Sunday et al.5.

Extended Data Fig. 3 Comparison of thermal limit divergence between motile and non-motile taxa.

Absolute difference in upper thermal limits between motile and non-motile taxa (motility defined here as whether or not an individual could control their microhabitat sufficiently to regulate body temperature using environmental thermal heterogeneity), calculated using both (a) unweighted raw mean differences (n = 215 non-motile & 269 motile) and (b) inverse-weighted standardized mean differences (Hedges’ g; n = 79 non-motile & 246 motile). Inset plots show the values for intertidal taxa alone. In all cases, the box plot’s horizontal line represents the median, while box limits illustrate the first and third quartiles. Whiskers extend from the box limits to the minimum and maximum values (not including outlier values that are more than 1.5 times the interquartile range from the box limits). Tables underneath each plot show the number of population pairs or effect size estimates for each realm and motility type.

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Supplementary Information

Supplementary Figs. 1–5.

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Supplementary Table 1

Contains the three Supplementary Tables as a single workbook with multiple tabs. Table legends are included on the first tab.

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Sasaki, M., Barley, J.M., Gignoux-Wolfsohn, S. et al. Greater evolutionary divergence of thermal limits within marine than terrestrial species. Nat. Clim. Chang. 12, 1175–1180 (2022). https://doi.org/10.1038/s41558-022-01534-y

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