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Complex parental effects impact variation in larval thermal tolerance in a vertically transmitting coral

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Abstract

Coral populations must be able to adapt to changing environmental conditions for coral reefs to persist under climate change. The adaptive potential of these organisms is difficult to forecast due to complex interactions between the host animal, dinoflagellate symbionts and the environment. Here we created 26 larval families from six Montipora capitata colonies from a single reef, showing significant, heritable variation in thermal tolerance. Our results indicate that 9.1% of larvae are expected to exhibit four times the thermal tolerance of the general population. Differences in larval thermotolerance were driven mainly by maternal contributions, but we found no evidence that these effects were driven by symbiont identity despite vertical transmission from the dam. We also document no evidence of reproductive incompatibility attributable to symbiont identity. These data demonstrate significant genetic variation within this population which provides the raw material upon which natural selection can act.

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Fig. 1: Wild-type larval dynamics under heat stress.
Fig. 2: Individual family responses.
Fig. 3: Relative family-wise performance under heat stress.
Fig. 4: Maternal and paternal performance under heat stress.
Fig. 5: Population phenotype frequencies support selective breeding.
Fig. 6: Symbiont community.

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Data availability

Data and code are uploaded to GitHub at: https://github.com/Erikacj/Matrix_reloaded.

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Acknowledgements

We gratefully acknowledge Hanalei Hoʻopai-Sylva, Khalil Smith, Josh Hancock, Madeleine Sherman, Maile Villablanca, Jasmine Chang, Ninah Munk, and the Coral Resilience Lab for spawning assistance. We also thank three anonymous reviewers for their edits and suggestions that improved this manuscript. This work was funded by the Paul G. Allen Family Foundation, NOAA Award NA20NMF4820290, and DARPA. Coral fragments and gamete bundles were collected under Hawaii DLNR permit SAP 2023-31 to HIMB. This is HIMB contribution 1949 and SOEST contribution 11780.

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Authors and Affiliations

  1. Hawai’i Institute of Marine Biology, University of Hawai’i, Kāne’ohe, HI, USA

    Erika C. Johnston, Carlo Caruso, Nia S. Walker & Crawford Drury

  2. Department of Bioengineering, University of California, Berkeley, CA, USA

    Elena Mujica

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Contributions

CC, ECJ and CD conceived the experiment. All authors collected data. ECJ and CD analyzed data. ECJ wrote the manuscript. All authors edited the manuscript and approved the final version.

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Correspondence to Erika C. Johnston.

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Johnston, E.C., Caruso, C., Mujica, E. et al. Complex parental effects impact variation in larval thermal tolerance in a vertically transmitting coral. Heredity (2024). https://doi.org/10.1038/s41437-024-00681-6

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