Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle

Forecasts of whether marine species can evolve fast enough to survive climate change rely largely on single-stage tolerance assays, tacitly assuming that tolerance measured at one developmental stage reflects adaptive capacity across the organism's life cycle. We test this assumption in a common marine bivalve (Mercenaria mercenaria) and find that it fails in sign, not degree: larval and post-metamorphic tolerance to end-century ocean acidification are strongly negatively correlated (r = -0.53, 95% CI [-0.69, -0.33]) across family-level, pedigree-conditioned and animal model estimates, with pervasive rank reversals among the top performers of each stage. A multivariate analysis of the among-family covariance matrix G shows why: under acidification, 57% of the among-family variance collapses onto a single dominant axis that loads positively on every larval trait and negatively on every post-metamorphic trait, whereas under ambient conditions the same families show no cross-stage covariance at all. Acidification therefore does not merely depress performance-it reorganizes the genetic architecture into a cross-stage conflict. Under ramping RCP 8.5 forcing this conflict geometry dictates the direction-not merely the magnitude-of adaptation: only balanced multi-stage selection preserves family diversity, whereas single-stage selection systematically erodes the opposite axis. In complex life cycles, resilience is a geometric property of ontogeny that forecasts cannot compress into a single-stage without inverting the sign of the answer.

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Publication Details

Journal
PLoS Biology
Published
2026-10-26
DOI
https://doi.org/10.1371/journal.pbio.3004079
Primary Topic
Ocean Acidification Effects and Responses
Type
article
Field-Weighted Citation Impact
0.00

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article

Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle

ANDREW G. JEFFS, Bassem Allam, Bradley M. Skelton, Hao Song et al.
PLoS Biology
Ocean Acidification Effects and Responses
article

Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle

ANDREW G. JEFFS, Bassem Allam, Bradley M. Skelton, Hao Song, Pu Shi, Tingyu Shi, Zhuoqing LI, Meijie Yang, Xiaoyan Liu, Tao Zhang, Yu Wu
article en

Abstract

Forecasts of whether marine species can evolve fast enough to survive climate change rely largely on single-stage tolerance assays, tacitly assuming that tolerance measured at one developmental stage reflects adaptive capacity across the organism's life cycle. We test this assumption in a common marine bivalve (Mercenaria mercenaria) and find that it fails in sign, not degree: larval and post-metamorphic tolerance to end-century ocean acidification are strongly negatively correlated (r = -0.53, 95% CI [-0.69, -0.33]) across family-level, pedigree-conditioned and animal model estimates, with pervasive rank reversals among the top performers of each stage. A multivariate analysis of the among-family covariance matrix G shows why: under acidification, 57% of the among-family variance collapses onto a single dominant axis that loads positively on every larval trait and negatively on every post-metamorphic trait, whereas under ambient conditions the same families show no cross-stage covariance at all. Acidification therefore does not merely depress performance-it reorganizes the genetic architecture into a cross-stage conflict. Under ramping RCP 8.5 forcing this conflict geometry dictates the direction-not merely the magnitude-of adaptation: only balanced multi-stage selection preserves family diversity, whereas single-stage selection systematically erodes the opposite axis. In complex life cycles, resilience is a geometric property of ontogeny that forecasts cannot compress into a single-stage without inverting the sign of the answer.

PLoS BiologyVol. 24(10)
Ningbo University (CN), University of Auckland (NZ), Chinese Academy of Sciences (CN), Institute of Oceanology (CN), University of Chinese Academy of Sciences (CN), Stony Brook University (US)
National Natural Science Foundation of China, Chinese Academy of Sciences, Youth Innovation Promotion Association of the Chinese Academy of Sciences, Taishan Scholar Foundation of Shandong Province, National Oceanic and Atmospheric Administration, Earmarked Fund for China Agriculture Research System, Young Scientists Fund, Youth Innovation Promotion Association, New York Sea Grant, State University of New York, NOAA Sea Grant
Openalex Percentile: Top 17%
Ocean Acidification Effects and Responses
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