Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Quantifying global potential for coral evolutionary response to climate change

Nature Climate Change volume 11, pages 537–542 (2021)Cite this article

Subjects

Abstract

Incorporating species’ ability to adaptively respond to climate change is critical for robustly predicting persistence. One such example could be the adaptive role of algal symbionts in setting coral thermal tolerance under global warming and ocean acidification. Using a global ecological and evolutionary model of competing branching and mounding coral morphotypes, we show symbiont shuffling (towards taxa with increased heat tolerance) was more effective than symbiont evolution in delaying coral-cover declines, but stronger warming rates (high emissions scenarios) outpace the ability of these adaptive processes and limit coral persistence. Acidification has a small impact on reef degradation rates relative to warming. Global patterns in coral reef vulnerability to climate are sensitive to the interaction of warming rate and adaptive capacity and cannot be predicted by either factor alone. Overall, our results show how models of spatially resolved adaptive mechanisms can inform conservation decisions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Percentage of ‘healthy’ reef cells globally in three RCP emissions scenarios from 1950 to 2100.
Fig. 2: Relative coral extent with and without symbiont-mediated adaptive capacity.
Fig. 3: Maps depicting the last year at which corals are projected to survive before the onset of high-frequency bleaching (≥2 events within the previous decade) or mortality.

Similar content being viewed by others

Code availability

All Matlab code can be found at https://github.com/VeloSteve/Coral-Model-V12 under the following: https://doi.org/10.5281/zenodo.2639126.

References

  1. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds Pörtner, H.-O. et al.) (IPCC, 2019).

  2. Urban, M. C. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).

    Article  CAS  Google Scholar 

  3. McCauley, D. J. & Pinsky, M. L. Marine defaunation: animal loss in the global ocean. Science 347, 1255641 (2015).

    Article  Google Scholar 

  4. Hoffmann, A. A. & Sgrò, C. M. Climate change and evolutionary adaptation. Nature 470, 479–485 (2011).

    Article  CAS  Google Scholar 

  5. Somero, G. N. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J. Exp. Biol. 213, 912–920 (2010).

    Article  CAS  Google Scholar 

  6. Kearney, M. & Porter, W. Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol. Lett. 12, 334–350 (2009).

    Article  Google Scholar 

  7. Foden, W. B. et al. Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS ONE 8, e65427 (2013).

    Article  CAS  Google Scholar 

  8. West, J. M. & Salm, R. V. Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv. Biol. 17, 956–967 (2003).

    Article  Google Scholar 

  9. Baskett, M. L., Nisbet, R. M., Kappel, C. V., Mumby, P. J. & Gaines, S. D. Conservation management approaches to protecting the capacity for corals to respond to climate change: a theoretical comparison. Glob. Change Biol. 16, 1229–1246 (2010).

    Article  Google Scholar 

  10. Beyer, H. L. et al. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 11, e12587 (2018).

    Article  Google Scholar 

  11. Walsworth, T. E. et al. Management for network diversity speeds evolutionary adaptation to climate change. Nat. Clim. Change 9, 632–636 (2019).

    Article  Google Scholar 

  12. Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    Article  CAS  Google Scholar 

  13. Donner, S. D., Skirving, W. J., Little, C. M., Oppenheimer, M. & Hoegh-Guldberg, O. Global assessment of coral bleaching and required rates of adaptation under climate change. Glob. Change Biol. 11, 2251–2265 (2005).

    Article  Google Scholar 

  14. Frieler, K. et al. Limiting global warming to 2 °C is unlikely to save most coral reefs. Nat. Clim. Change 3, 165–170 (2012).

    Article  Google Scholar 

  15. Van Hooidonk, R., Maynard, J. A., Manzello, D. & Planes, S. Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Glob. Change Biol. 20, 103–112 (2014).

    Article  Google Scholar 

  16. Logan, C. A., Dunne, J. P., Eakin, C. M. & Donner, S. D. Incorporating adaptive responses into future projections of coral bleaching. Glob. Change Biol. 20, 125–139 (2014).

    Article  Google Scholar 

  17. Bay, R. A., Rose, N. H., Logan, C. A. & Palumbi, S. R. Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Sci. Adv. 3, e1701413 (2017).

    Article  Google Scholar 

  18. Matz, M. V., Treml, E. A. & Haller, B. C. Estimating the potential for coral adaptation to global warming across the Indo-West Pacific. Glob. Change Biol. 26, 3473–3481 (2020).

    Article  Google Scholar 

  19. Baskett, M. L., Gaines, S. D. & Nisbet, R. M. Symbiont diversity may help coral reefs survive moderate climate change. Ecol. Appl. 19, 3–17 (2009).

    Article  Google Scholar 

  20. Matz, M. V., Treml, E. A., Aglyamova, G. V. & Bay, L. K. Potential and limits for rapid genetic adaptation to warming in a Great Barrier Reef coral. PLoS Genet. 14, e1007220 (2018).

    Article  Google Scholar 

  21. Muscatine, L., Falkowski, P. G., Porter, J. W. & Dubinsky, Z. Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. Lond. B. 222, 181–202 (1984).

    Article  CAS  Google Scholar 

  22. Csaszar, N. B., Ralph, P. J., Frankham, R., Berkelmans, R. & van Oppen, M. J. Estimating the potential for adaptation of corals to climate warming. PLoS ONE 5, e9751 (2010).

    Article  Google Scholar 

  23. Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Change 2, 116–120 (2012).

    Article  Google Scholar 

  24. Buerger, P. et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci. Adv. 6, eaba2498 (2020).

    Article  CAS  Google Scholar 

  25. Baker, A. C. Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661–689 (2003).

  26. Berkelmans, R. & van van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. Lond. B 273, 2305–2312 (2006).

    Google Scholar 

  27. National Academies of Sciences, Engineering, and Medicine A research Review of Interventions to Increase the Persistence and Resilience of Coral Reefs (National Academies Press, 2019).

  28. National Academies of Sciences, Engineering, and Medicine A Decision Framework for Interventions to Increase the Persistence and Resilience of Coral Reefs (National Academies Press, 2019).

  29. Darling, E. S., Alvarez-Filip, L., Oliver, T. A., McClanahan, T. R. & Côté, I. M. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15, 1378–1386 (2012).

    Article  Google Scholar 

  30. Chan, N. C. S. & Connolly, S. R. Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob. Change Biol. 19, 282–290 (2013).

    Article  Google Scholar 

  31. Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).

    Article  CAS  Google Scholar 

  32. Darling, E. S. et al. Relationships between structural complexity, coral traits, and reef fish assemblages. Coral Reefs 36, 561–575 (2017).

    Article  Google Scholar 

  33. Howells, E. J. et al. Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol. 29, 899–911 (2020).

    Article  CAS  Google Scholar 

  34. Madin, J. S., Hughes, T. P. & Connolly, S. R. Calcification, storm damage and population resilience of tabular corals under climate change. PLoS ONE 7, e46637 (2012).

    Article  CAS  Google Scholar 

  35. Hoegh-Guldberg, O. et al. in Global Warming of 1.5°C (eds Masson-Delmotte, V. et al.) Ch. 3 (IPCC, 2018).

  36. Darling, E. S. et al. Social–environmental drivers inform strategic management of coral reefs in the Anthropocene. Nat. Ecol. Evol. 3, 1341–1350 (2019).

    Article  Google Scholar 

  37. Wilkinson, C. R. Global and local threats to coral reef functioning and existence: review and predictions. Mar. Freshw. Res. 50, 867–878 (1999).

    Google Scholar 

  38. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014).

    Article  CAS  Google Scholar 

  39. Kleypas, J. A. et al. Larval connectivity across temperature gradients and its potential effect on heat tolerance in coral populations. Glob. Change Biol. 22, 3539–3549 (2016).

    Article  Google Scholar 

  40. Heron, S. F. et al. Validation of reef-scale thermal stress satellite products for coral bleaching monitoring. Remote Sens. 8, 59 (2016).

    Article  Google Scholar 

  41. Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).

    Article  Google Scholar 

  42. Forster, P. M. et al. Evaluating adjusted forcing and model spread for historical and future scenarios in the CMIP5 generation of climate models. J. Geophys. Res. Atmos. 118, 1139–1150 (2013).

    Article  Google Scholar 

  43. Ziegler, M., Eguíluz, V. & Duarte, C. et al. Rare symbionts may contribute to the resilience of coral–algal assemblages. ISME J 12, 161–172 (2018).

    Article  Google Scholar 

  44. Sampayo, E. M., Ridgway, T., Bongaerts, P. & Hoegh-Guldberg, O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc. Natl Acad. Sci. USA 105, 10444–10449 (2008).

    Article  CAS  Google Scholar 

  45. Thornhill, D. J., Xiang, Y. U., Fitt, W. K. & Santos, S. R. Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 4, e6262 (2009).

    Article  Google Scholar 

  46. Stat, M., Loh, W. K. W., LaJeunesse, T. C., Hoegh-Guldberg, O. & Carter, D. A. Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28, 709–713 (2009).

    Article  Google Scholar 

  47. Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Change Biol. 23, 4675–4688 (2017).

    Article  Google Scholar 

  48. Schulte, P. M., Healy, T. M. & Fangue, N. A. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr. Comp. Biol. 51, 691–702 (2011).

    Article  Google Scholar 

  49. Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131 (2001).

    Article  Google Scholar 

  50. Langmead, O. & Sheppard, C. Coral reef community dynamics and disturbance: a simulation model. Ecol. Modell. 175, 271–290 (2004).

    Article  Google Scholar 

  51. Chancerelle, Y. Methods to estimate actual surface areas of scleractinian coral at the colony- and community-scale. Oceanol. Acta 23, 211–219 (2000).

    Article  Google Scholar 

  52. Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984).

    Article  CAS  Google Scholar 

  53. Huston, M. Variation in coral growth rates with depth at Discovery Bay, Jamaica. Coral Reefs 4, 19–25 (1985).

    Article  Google Scholar 

  54. Hoogenboom, M., Beraud, E. & Ferrier-Pagès, C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29, 21–29 (2010).

    Article  Google Scholar 

  55. Cunning, R. & Baker, A. C. Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front. Microbiol. 5, 400 (2014).

    Article  Google Scholar 

  56. McClanahan, T., Muthiga, N. & Mangi, S. Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs 19, 380–391 (2001).

    Article  Google Scholar 

  57. Fitt, W. K., McFarland, F. K., Warner, M. E. & Chilcoat, G. C. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 45, 677–685 (2000).

    Article  CAS  Google Scholar 

  58. Eppley, R. W. Temperature and phytoplankton growth in the sea. Fish. Bull. 70, 1063–1085 (1972).

    Google Scholar 

  59. Jon, N. Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnol. Oceanogr. 49, 1269–1277 (2004).

    Article  Google Scholar 

  60. Mousseau, T. A. & Roff, D. A. Natural selection and the heritability of fitness components. Heredity 59, 181–197 (1987).

    Article  Google Scholar 

  61. Lynch, M. The rate of polygenic mutation. Genet. Res. 51, 137–148 (1988).

    Article  CAS  Google Scholar 

  62. Donner, S. D., Rickbeil, G. J. & Heron, S. F. A new, high-resolution global mass coral bleaching database. PLoS ONE 12, e0175490 (2017).

    Article  Google Scholar 

  63. Cunning, R., Gillette, P., Capo, T., Galvez, K. & Baker, A. C. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34, 155–160 (2015).

    Article  Google Scholar 

  64. Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Change Biol. 21, 236–249 (2015).

    Article  Google Scholar 

  65. Dunne, J. P. et al. GFDL’s ESM2 global coupled climate–carbon Earth system models part I: physical formulation and baseline simulation characteristics. J. Clim. 25, 6646–6665 (2012).

    Article  Google Scholar 

  66. Dunne, J. P. et al. GFDL’s ESM2 global coupled climate–carbon Earth system models Part II: carbon system formulation and baseline simulation characteristics. J. Clim. 26, 2247–2267 (2012).

    Article  Google Scholar 

  67. Lough, J. M. & Barnes, D. J. Environmental controls on growth of the massive coral Porites. J. Exp. Mar. Biol. Ecol. 245, 225–243 (2000).

    Article  CAS  Google Scholar 

  68. UNEP-WCMC, WorldFish Centre, WRI & TNC. Global Distribution of Warm-water Coral Reefs, Compiled From Multiple Sources Including the Millennium Coral Reef Mapping Project. Version 4.1 (UN Environment World Conservation Monitoring Centre. Data, 2021); https://doi.org/10.34892/t2wk-5t34

  69. van Hooidonk, R., Maynard, J. A. & Planes, S. Temporary refugia for coral reefs in a warming world. Nat. Clim. Change 3, 508–511 (2013).

    Article  Google Scholar 

  70. Fitt, W., Brown, B., Warner, M. & Dunne, R. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65 (2001).

    Article  Google Scholar 

  71. González-Espinosa, P. C. & Donner, S. D. Predicting cold-water bleaching in corals: role of temperature, and potential integration of light exposure. Mar. Ecol. Prog. Ser. 642, 133–146 (2020).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a NOAA Coral Reef Conservation grant to J.P.D. and S.D.D., a Coral Reef Alliance Coral Adaptation Challenge grant to C.A.L. and S.D.D., and an ROA supplement to NSF DEB #1655475 to C.A.L. and M.L.B. We thank C. M. Eakin for helpful initial discussions in the development of the global model. The contents in this manuscript are solely the opinions of the authors and do not constitute a statement of policy, decision or position on behalf of NOAA or the US Government.

Author information

Authors and Affiliations

  1. Department of Marine Science, California State University, Monterey Bay, Seaside, CA, USA

    Cheryl A. Logan & James S. Ryan

  2. NOAA/OAR Geophysical Fluid Dynamics Laboratory, Princeton, NJ, USA

    John P. Dunne

  3. Department of Environmental Science and Policy, University of California Davis, Davis, CA, USA

    Marissa L. Baskett

  4. Department of Geography, University of British Columbia, Vancouver, British Columbia, Canada

    Simon D. Donner

Authors
  1. Cheryl A. Logan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John P. Dunne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James S. Ryan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marissa L. Baskett
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simon D. Donner
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.A.L., J.P.D. and S.D.D. conceived and designed the global model; C.A.L. and J.S.R. developed and tested the computer code; C.A.L., J.P.D., J.S.R. and S.D.D. analysed the results; C.A.L. and J.S.R. wrote the paper. C.A.L., J.P.D., J.S.R., S.D.D. and M.L.B. critically revised the manuscript.

Corresponding author

Correspondence to Cheryl A. Logan.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Climate Change thanks M. Matz and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Coral and symbiont ecological and evolutionary global model diagram.

The left-hand boxes (a) describe the symbiont fitness curve and genetic dynamics. The right-hand boxes (b) describe the coral and symbiont population dynamics.

Extended Data Fig. 2 Relative coral extent across all reef cells in a 400-year model run with no anthropogenic warming and no adaptive capacity.

In all model runs, branching corals (blue) are initialized at 80% and mounding corals (red) at 20% of a fixed pre-warming carrying capacity (K) in 1861 averaged across all reef cells. Initializing coral morphotypes to the inverse of these proportions (80% mounding: 20% branching) results in a similar outcome (~ 90% branching and 1% mounding corals) by 1950. Shaded colors represent the 50% interquartile range around the mean for all reef cells.

Extended Data Fig. 3 Percentage of ‘healthy’ reef cells globally in four RCP emissions scenarios from 1980 to 2100.

Model trajectories are shown with no evolution (black), shuffling with a +1 °C advantage (red), evolution (blue), and combined shuffling and evolution (purple). A reef is considered ‘healthy’ if it is not in a bleached or mortality state (see Methods). SST (grey) is the mean and 25th-75th percentile increase in annual maximum temperatures across all reef grid cells. Bar plots indicate number of bleaching events per year in each model run.

Extended Data Fig. 4 In each model year, reef cells are defined as being in a ‘healthy’, ‘bleached’, or ‘mortality’ state.

Arrows represent transitions between states. 1) ‘Bleaching’ occurs when symbiont populations drop <30% of the minimum population size in the previous year or when bleaching occurs ≥2 times in the previous decade. 2) ‘Mortality’ is defined if a reef bleaches but does not recover within five years, or 3) if coral populations drop to <2x the seed value. 4-5) Recovery occurs if coral and symbiont populations increase to >4x their respective seed value or coral populations grow above 10% of carrying capacity.

Extended Data Fig. 5 Sensitivity analysis of percent ‘healthy’ coral reef cells when the model is calibrated to estimated bleaching frequencies of 3 or 5% between 1985-2010.

In the main text, model output is calibrated to a 5% bleaching frequency during this time. The effect of changing the target to 3 % is shown for RCP4.5 and RCP8.5 scenarios. Projected trajectories are shown with and without symbiont evolution (E=1 vs. E=0), and with or without shuffling (+1.0 °C advantage) in the tolerant population. The effect of increasing pCO2 on coral growth rates is also included (OA=1) with evolution and shuffling.

Extended Data Fig. 6 Global mean fraction of corals hosting heat-tolerant symbionts in branching (heat-sensitive) corals and mounding (heat-tolerant) corals.

The mean value is calculated for all reef cells (n=1,925) for all RCPs in shuffling (+1.0 °C advantage) simulations. For most reefs, fidelity to heat-tolerant symbiont occurs following a rapid transition between 2010-2040 through 2100.

Extended Data Fig. 7 Fine-scale symbiont shuffling dynamics in four example reef cells.

Temperature is monthly SST with the optimal temperature (gi) for each symbiont type overlaid in yellow (top). Symbiont density (bottom) is in terms of cells per cm2 of coral area for a heat-sensitive (solid lines) and heat-tolerant (dashed lines) symbiont population in each coral morphotype. Realistic seasonal fluctuations in symbiont density (a,b) and reversion can occur (c, d), but reversion is uncommon under future warming; (d) represents a model run with no anthropogenic warming in which reversion occurs several times during a 200-year period. Bleaching events are shown in black circles.

Extended Data Fig. 8 Global change in mean symbiont genotype (gi or optimal temperature in °C) and average increase in annual maximum sea surface temperatures (SST) in model runs with symbiont evolution for all RCPs.

Median (solid lines) and interquartile range (shaded) is shown across all reef cells (n=1,925) for mounding (heat-tolerant) and branching (heat-sensitive) corals. Across all RCP scenarios and all reefs, the increase in symbiont optimal thermal tolerance ranged between 0.3°C and 1.8°C.

Extended Data Fig. 9 Global maps of warming rate and SST variability.

Values represent change in each temperature metric between the historical period (1861-1900) and 2080 (a-d, g-h) as well as future variability between 2050-2080 (e-f, i-j) for RCP 4.5 and RCP 8.5 climate scenarios. In panels (a) to (f), inputs are filtered to include only maximum monthly mean SST. Panels (g) through (j) include all months.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Logan, C.A., Dunne, J.P., Ryan, J.S. et al. Quantifying global potential for coral evolutionary response to climate change. Nat. Clim. Chang. 11, 537–542 (2021). https://doi.org/10.1038/s41558-021-01037-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41558-021-01037-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing