Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle
8 affiliations
- 1Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
- 2School of Marine Sciences, Ningbo University, Ningbo, China
- 3Laboratory for Marine Ecology and Environmental Science, Qingdao Marine Science and Technology Center, Qingdao, China
- 4State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
- 5University of Chinese Academy of Sciences, Beijing, China
- 6Marine Animal Disease Laboratory, School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, United States of America
- 7Institute of Marine Science, University of Auckland, Auckland, New Zealand
- 8Lianyungang Zhongke Meibei Marine Technology Co., Ltd, Lianyungang, China
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.
Forecasts of whether marine species can survive climate change rely largely on tolerance assays at one developmental stage. This study of the tolerance of an animal with a complex life cycle to end-century ocean acidification reveals cross-stage conflicts that impact the direction and magintude of adaptation.
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BibTeX
@article{song2026tolerance,
title = {{Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle}},
author = {Hao Song and Tingyu Shi and Meijie Yang and Xiaoyan Liu and Zhuoqing Li and Pu Shi and Yu Wu and Bassem Allam and Andrew Jeffs and Bradley Skelton and Tao Zhang},
journal = {PLOS Biology},
year = {2026},
month = oct,
doi = {10.1371/journal.pbio.3004079},
url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004079},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Tolerance measured at one developmental stage mispredicts climate resilience in an animal with a complex life cycle
AU - Hao Song
AU - Tingyu Shi
AU - Meijie Yang
AU - Xiaoyan Liu
AU - Zhuoqing Li
AU - Pu Shi
AU - Yu Wu
AU - Bassem Allam
AU - Andrew Jeffs
AU - Bradley Skelton
AU - Tao Zhang
PY - 2026
DA - 2026/10/26
JO - PLOS Biology
DO - 10.1371/journal.pbio.3004079
UR - https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004079
AB - 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. Forecasts of whether marine species can survive climate change rely largely on tolerance assays at one developmental stage. This study of the tolerance of an animal with a complex life cycle to end-century ocean acidification reveals cross-stage conflicts that impact the direction and magintude of adaptation.
SN - 1545-7885
SN - 1544-9173
ER -