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Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification

Abstract

Predicting the response of marine animals to climate change is hampered by a lack of multigenerational studies on evolutionary adaptation, particularly to combined ocean warming and acidification (OWA). We provide evidence for rapid adaptation to OWA in the foundational copepod species, Acartia tonsa, by assessing changes in population fitness on the basis of a comprehensive suite of life-history traits, using an orthogonal experimental design of nominal temperature (18 °C, 22 °C) and \(p_{\mathrm{{CO}}_2}\) (400, 2,000 µatm) for 25 generations (~1 year). Egg production and hatching success initially decreased under OWA, resulting in a 56% reduction in fitness. However, both traits recovered by the third generation, and average fitness was reduced thereafter by only 9%. Antagonistic interactions between warming and acidification in later generations decreased survival, thereby limiting full fitness recovery. Our results suggest that such interactions constrain evolutionary rescue and add complexity to predictions of the responses of animal populations to climate change.

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Fig. 1: Changes in EPR and HS during the transgenerational experiment.
Fig. 2: Changes in survival during the transgenerational study.
Fig. 3: Mean fitness values, λ, calculated for the transgenerational study.
Fig. 4: Fitness landscapes showing trait contribution to adaptation during the transgenerational experiment.

Data availability

The phenotypic and physical data referred to in the text are deposited in Zenodo (https://doi.org/10.5281/zenodo.5119920)75. The genetic diversity data are deposited in GenBank: BioProject number PRJNA590963. Source data are provided with this paper.

Code availability

The scripts for analysis of the physical, phenotypic and genetic diversity data are deposited in Zenodo (https://doi.org/10.5281/zenodo.5119920).

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Acknowledgements

Research was supported by grants from the USA National Science Foundation (OCE-1559180 awarded to H.G.D., M.B.F. and H.B.; and OCE-1559075 awarded to M.H.P.) and Connecticut Sea Grant (R/LR‐25) awarded to H.G.D., M.B.F. and H.B. The authors thank W. Huffman for aiding in pilot experiments; C. Murray for assistance in alkalinity measurements; D. Arbige, C. Woods and B. Dziomba for help in maintaining equipment and constructing custom enclosures for the experiments; and T. Moore and J. Lee of UConn’s Statistical Consulting Services for advice and assistance on data analysis.

Author information

Authors and Affiliations

Authors

Contributions

H.G.D. conceived the project, designed research, aided in data analysis and wrote the manuscript. J.A.deM. conducted experiments, analysed data, created figures and wrote the manuscript with H.G.D. G.P., L.N. and X.H. conducted experiments. M.B.F. conceived the project and designed research. H.B. conceived the project, designed research and designed the CO2 delivery system. R.S.B. performed genomic diversity analysis. M.H.P. conceived the project, designed research and performed genomic analysis. All authors edited and approved the paper.

Corresponding authors

Correspondence to Hans G. Dam or James A. deMayo.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Peter Thor 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 Development time vs generation for transgenerational study.

Shown are the mean calculated development times (naupliar stage 1 to adult) for each treatment at each generation where life-history traits are measured. Curves for treatments are offset for clarity. Treatment colors: blue: AM; green: OA; orange: OW; brown: OWA. Box and whisker plots for these data are available in Supplemental Fig. 4.

Source data

Extended Data Fig. 2 Sex ratio vs generation for transgenerational study.

Results for sex ratio across generations modeled as A) linear model and B) Generalized Additive Model. Treatment colors: blue: AM; green: OA; orange: OW; brown: OWA.

Source data

Extended Data Fig. 3 Frequency distribution of population fitness values (λ) for the four treatments in the transgenerational experiment.

Treatment colors: blue: AM; green: OA; orange: OW; brown: OWA.

Source data

Extended Data Fig. 4 Predicted probabilities of non-zero fitness (lambda) values vs generations across treatments in the transgenerational experiment.

Shown are predicted mean non-zero lambda probabilities. Probabilities for ambient (AM), ocean acidification (OA), and ocean warming (OW) treatments are statistically independent of generations. Probabilities for the simultaneous ocean warming and acidification (OWA) significantly increase with generation. Shading represents 95% confidence intervals around the mean. Treatment colors: blue: AM; green: OA; orange: OW; brown: OWA.

Source data

Extended Data Fig. 5 Estimates of genetic diversity (π) at generation 25 vs treatments of the transgenerational experiment.

Estimates were calculated in 100 bp non-overlapping sliding windows. Windows were included when at least 50% of sites had coverage between 30x and 1000x per sample and the window was covered across all samples. The asterisk indicates the sample in the OA treatment with reduced genetic diversity relative to other samples (Wilcoxon Rank Sum test with Holm correction for multiple testing; p < 0.05); all other samples were not significantly different (p > 0.05). In the boxes, the centre black line represents the median, the circles represent means, upper box edge represents the 75% quartile, lower box edge represents 25% quartile, whiskers represent 1.5x interquartile range, and points represent outliers. Treatment colors: blue: AM; green: OA; orange: OW; brown: OWA.

Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–4 and Tables 1–5.

Reporting Summary

Source data

Source Data Fig. 1

Unprocessed values of egg production and hatching success.

Source Data Fig. 2

Unprocessed values for survival.

Source Data Fig. 3

Unprocessed values for fitness (λ).

Source Data Fig. 4

Sheet 1: Table of fitness (λ) and relative fitness values with corresponding survival, egg production, hatching success, development time and sex ratio values for the first and last evaluated generations. Sheet 2: Table of survival values for the first and last generations.

Source Data Extended Data Fig. 1

Unprocessed values for calculated development time.

Source Data Extended Data Fig. 2

Unprocessed values for observed sex ratio (proportion of females relative to males).

Source Data Extended Data Fig. 3

Unprocessed values for fitness (λ).

Source Data Extended Data Fig. 4

Unprocessed values for fitness (λ) with binary transformed λ. λ values > 0 are given a binary value of 1, and λ values = 0 are given a binary value of 0.

Source Data Extended Data Fig. 5

Unprocessed values of nucleotide diversity for F25.

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Dam, H.G., deMayo, J.A., Park, G. et al. Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification. Nat. Clim. Chang. 11, 780–786 (2021). https://doi.org/10.1038/s41558-021-01131-5

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