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Coral thermal tolerance shaped by local adaptation of photosymbionts

Abstract

Coral thermal tolerance is strongly influenced by the identity of obligate photosymbionts, which encompass numerous types belonging to the dinoflagellate genus Symbiodinium1. Physiological advantages achieved by partnering with functionally diverse symbionts2,3,4 have been assumed to be available only to corals that can form associations with multiple Symbiodinium types. Functional variation among populations of the same type of Symbiodinium has been overlooked, despite local adaptation being feasible because of large population sizes5,6, genetic isolation7,8 and short asexual generation times9. Here we demonstrate divergent thermal tolerance in a generalist Symbiodinium type from two different thermal environments. Symbiodinium from the warmer reef maintained greater photo-chemical performance and survivorship when exposed to an elevated temperature of 32 °C, both in symbiosis and in culture. Juvenile corals associated with Symbiodinium from the warmer reef grew rapidly when exposed to 32 °C, yet underwent bleaching and tissue death when associated with Symbiodinium from the cooler reef. These results demonstrate that Symbiodinium types can adapt to local differences in thermal climate and that this adaptation shapes the fitness of coral hosts. If Symbiodinium populations are able to further adapt to increases in temperature at the pace at which ocean climates warm, they may assist corals to increase their thermal tolerance and persist into the future.

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Figure 1: Location and summer temperature trends of Symbiodinium C1 populations (red, blue) and location of the A. millepora coral population (black) on the Great Barrier Reef, Australia.
Figure 2: Responses of Symbiodinium–Acropora millepora symbioses to ambient and elevated temperature.
Figure 3: Symbiodinium C1 population responses to ambient and elevated temperatures following one year of growth in cell cultures.

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References

  1. Coffroth, M. A. & Santos, S. R. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist. 156, 19–34 (2005).

    Article  CAS  Google Scholar 

  2. Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Corals’ adaptive response to climate change. Nature 430, 741 (2004).

    Article  CAS  Google Scholar 

  3. Rowan, R. Coral bleaching—thermal adaptation in reef coral symbionts. Nature 430, 742 (2004).

    Article  CAS  Google Scholar 

  4. Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: Field evidence of acclimatization. Proc. R. Soc. B 275, 1359–1365 (2008).

    Article  CAS  Google Scholar 

  5. Drew, E. A. The biology and physiology of alga invertebrate symbioses. Part 2. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. J. Exp. Mar. Biol. Ecol. 9, 71–75 (1972).

    Article  Google Scholar 

  6. Littman, R. A., van Oppen, M. J. H. & Willis, B. L. Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J. Exp. Mar. Biol. Ecol. 364, 48–53 (2008).

    Article  Google Scholar 

  7. Santos, S. R., Gutierrez-Rodriguez, C., Lasker, H. R. & Coffroth, M. A. Symbiodinium sp associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: High levels of genetic variability and population structure in symbiotic dinoflagellates. Mar. Biol. 143, 111–120 (2003).

    Article  Google Scholar 

  8. Howells, E. J., van Oppen, M. J. H. & Willis, B. L. High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28, 215–225 (2009).

    Article  Google Scholar 

  9. Wilkerson, F. P., Kobayashi, D. & Muscatine, L. Mitotic index and the size of symbiotic algae in Caribbean reef corals. Coral Reefs 7, 29–36 (1988).

    Article  Google Scholar 

  10. Richmond, R. H. in Life Death Coral Reefs (ed. Birklund, C.) 175–197 (Springer, 1997).

    Book  Google Scholar 

  11. LaJeunesse, T. C. et al. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284, 147–161 (2004).

    Article  Google Scholar 

  12. Cooper, T. F. et al. Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS ONE 6, e25536 (2011).

    Article  CAS  Google Scholar 

  13. Goulet, T. L., Simmons, C. & Goulet, D. Worldwide biogeography of Symbiodinium in tropical octocorals. Mar. Ecol. Prog. Ser. 355, 45–58 (2008).

    Article  Google Scholar 

  14. Wicks, L. C., Sampayo, E., Gardner, J. P. A. & Davy, S. K. Local endemicity and high diversity characterize high-latitude coral-Symbiodinium partnerships. Coral Reefs 29, 989–1003 (2010).

    Article  Google Scholar 

  15. LaJeunesse, T. C. ‘Species’ radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol. 22, 570–581 (2005).

    Article  CAS  Google Scholar 

  16. Schaffelke, B. et al. Water quality in the inshore Great Barrier Reef lagoon: Implications for long-term monitoring and management. Mar. Pollut. Bull. (in the press).

  17. Siefermann-Harms, D. The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol. Planta. 69, 561–568 (1987).

    Article  CAS  Google Scholar 

  18. Goulet, T. L. & Coffroth, M. A. Stability of an octocoral-algal symbiosis over time and space. Mar. Ecol. Prog. Ser. 250, 117–124 (2003).

    Article  Google Scholar 

  19. Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).

    Article  Google Scholar 

  20. Goulet, T. L., LaJeunesse, T. C. & Fabricius, K. E. Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar. Biol. 154, 795–804 (2008).

    Article  Google Scholar 

  21. Thornhill, D. J., Xiang, Y., 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 

  22. Jones, A. & Berkelmans, R. Potential costs of acclimatization to a warmer climate: Growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5, e10437 (2010).

    Article  Google Scholar 

  23. Abrego, D., Ulstrup, K. E., Willis, B. L. & van Oppen, M. J. H. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc. R. Soc. B 275, 2273–2282 (2008).

    Article  CAS  Google Scholar 

  24. Meyer, J. R., Ellner, S. P., Hairston, N. G., Jones, L. E. & Yoshida, T. Prey evolution on the timescale of predator–prey dynamics revealed by allele-specific quantitative PCR. Proc. Natl Acad. Sci. USA 103, 10690–10695 (2006).

    Article  CAS  Google Scholar 

  25. Costas, E., Flores-Moya, A. & Lopez-Rodas, V. Rapid adaptation of phytoplankters to geothermal waters is achieved by single mutations: were extreme environments ‘Noah’s Arks’ for photosynthesizers during the Neoproterozoic ‘snowball Earth’? New Phytol. 180, 922–932 (2008).

    Article  Google Scholar 

  26. Buddemeier, R. W. & Fautin, D. G. Coral bleaching as an adaptive mechanism—a testable hyspothesis. Bioscience 43, 320–326 (1993).

    Article  Google Scholar 

  27. Correa, A. M. S. & Baker, A. C. Disaster taxa in microbially mediated metazoans: How endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob. Change Biol. 17, 68–75 (2011).

    Article  Google Scholar 

  28. Voolstra, C. R. et al. Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium). Comput. Biochem. Physiol. D 4, 67–74 (2009).

    Google Scholar 

  29. Cantin, N. E., van Oppen, M. J. H., Willis, B. L., Mieog, J. C. & Negri, A. P. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28, 405–414 (2009).

    Article  Google Scholar 

  30. Mieog, J. C. et al. The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4, e6364 (2009).

    Article  Google Scholar 

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Acknowledgements

The Centre for Marine Microbiology and Genetics at the Australian Institute of Marine Science provided aquarium facilities and M. Salmon, J. Hochen, R. Berkelmans, D. Bourne and E. Puill-Stephan assisted with set-up or materials. R. Berkelmans and L. Tonk provided information on the distribution of Symbiodinium types on the Great Barrier Reef. J. White, J. Tan, S. Gardner, P. Warner, M. Condy, A. Moya and A. Baird assisted with fieldwork. J. Doyle, A. Negri, V. Cumbo and S. Uthicke provided technical advice on pigment analysis, coral larval rearing, Symbiodinium inoculation and chlorophyll fluorescence. The study was funded by an Australian Research Council grant to B.L.W. and M.J.H.v.O., an AIMS@JCU grant to E.J.H., and a Marine and Tropical Sciences Research Facility grant to B.L.W., M.J.H.v.O. and L.K.B.

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E.J.H. designed the study, collected and analysed data, and wrote the manuscript. L.K.B., B.L.W. and M.J.H.v.O. contributed to study design and manuscript writing. V.H.B. originated and maintained Symbiodinium cultures. N.W.L. assisted with field and laboratory work. All authors discussed the results and commented on the manuscript.

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Correspondence to E. J. Howells.

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The authors declare no competing financial interests.

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Howells, E., Beltran, V., Larsen, N. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim Change 2, 116–120 (2012). https://doi.org/10.1038/nclimate1330

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