Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1696, 2010, Pages 2925-2934

  LaJeunesse, Todd C ^a   Smith, Robin ^b   Walther, Mariana ^c   Pinzón, Jorge ^a   Pettay, Daniel T ^a   McGinley, Michael ^d   Aschaffenburg, Matthew ^d   Medina Rosas, Pedro ^e   Cupul Magaña, Amilcar L ^e   Pérez, Andrés López ^f   Reyes Bonilla, Hector ^c   Warner, Mark E ^d  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^c UNIVERSIDAD AUTÓNOMA DE BAJA CALIFORNIA SUR   (Mexico)

^d UNIVERSITY OF DELAWARE   (United States)

^e UNIVERSITY OF GUADALAJARA   (Mexico)

^f UNIVERSIDAD DEL MAR   (Mexico)

Author keywords

Climate change; Coral bleaching; Eastern Pacific; Holobiont; Natural selection; Symbiodinium

Indexed keywords

ALGA; CLIMATE CHANGE; CORAL; CORAL BLEACHING; DINOFLAGELLATE; EL NINO-SOUTHERN OSCILLATION; ENDOSYMBIONT; ENVIRONMENTAL DISTURBANCE; GLOBAL CLIMATE; HOST-SYMBIONT INTERACTION; INVASIVE SPECIES; MORTALITY; MUTUALISM; NATURAL SELECTION; POLYP; TURBIDITY;

FEDERAL DISTRICT [MEXICO]; GULF OF CALIFORNIA; MEXICO CITY; MEXICO [NORTH AMERICA]; PACIFIC OCEAN;

AIPTASIA; ALGAE; ANEMONE; ANTHOZOA; DINOPHYCEAE; POCILLOPORA; SYMBIODINIUM;

EID: 77956906680     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0385     Document Type: Conference Paper

References (63)

1. Adl, S. M. et al. 2007 Diversity, nomenclature, and taxonomy of Protists. Syst. Biol. 56, 684-689. (doi:10.1080/ 10635150701494127)
2. Baird, H. A., Bhagooli, R., Ralph, P. J. & Takahashi, S. 2009 Coral bleaching: the role of the host. Trends Ecol. Evol. 24, 16-20. (doi:10.1016/j.tree.2008.09.005)
3. Baker, A. C. 2001 Reef corals bleach to survive change. Nature 411, 765-766. (doi:10.1038/35081151) (Pubitemid 32588090)
4. Baker, A. C. 2003 Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661-689. (doi:10.1146/annurev.ecolsys.34.011802.132417)
5. Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. 2004 Corals' adaptive response to climate change. Nature 430, 741. (doi:10.1038/430741a) (Pubitemid 39071337)
6. Barshis, D. J., Stillman, J. H., Gates, R. D., Toonen, R. J., Smith, L. W. & Birkeland, C. 2010 Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol. Ecol. 19, 1705-1720. (doi:10.1111/j.1365-294X.2010.04574.x)
7. Berkelmanns, R. & van Oppen, M. J. H. 2006 Flexible partners in coral symbiosis: a 'nugget of hope' for coral reefs in an era of climate change. Proc. R. Soc. B 273, 2305-2312. (doi:10.1098/rspb.2006.3567) (Pubitemid 44387337)
8. Budd, A. 2000 Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19, 25-35. (doi:10.1007/s003380050222)
9. Carroll, S. P., Hendry, A. P., Reznick, D. N. & Fox, C. W. 2007 Evolution on ecological time-scales. Funct. Ecol. 21, 387-393. (doi:10.1111/j.1365-2435.2007.01289.x) (Pubitemid 46802147)
10. Coles, S. L. & Brown, B. E. 2003 Coral bleaching-capacity for acclimatization and adaptation. Adv. Mar. Biol. 46, 183-223. (doi:10.1016/S0065-2881(03)46004-5) (Pubitemid 38851782)
11. Correa, A. M. S., McDonald, M. D. & Baker, A. C. 2009 Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar. Biol. 156, 2403-2411. (doi:10.1007/s00227-009-1263-5)
12. Fitt, W. K., Brown, B. E., Warner, M. E. & Dunne, R. P. 2001 Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51-65. (doi:10.1007/s003380100146) (Pubitemid 32770401)
13. Glynn, P. W. 1983 Extensive 'bleaching' and death of reef corals on the Pacific coast of Panamá. Environ. Conserv. 10, 149-154. (doi:10.1017/S0376892900012248)
14. Glynn, P. W. 1993 Coral bleaching: ecological perspectives. Coral Reefs 12, 1-17. (doi:10.1007/BF00303779)
15. Glynn, P. W. & Ault, J. S. 2000 A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19, 1-23. (doi:10.1007/s003380050220)
16. Glynn, P. W., Mate, J. L., Baker, A. C. & Calderon, M. O. 2001 Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Niño-Southern oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bull. Mar. Sci. 69, 79-109.
17. Goulet, T. L. 2006 Most corals may not change their sym-bionts. Mar. Ecol. Prog. Ser. 321, 1-7. (doi:10.3354/ meps321001)
18. Goulet, T. L. & Coffroth, M. A. 2003 Stability of an octocoral-algal symbiosis over time and space. Mar. Ecol. Prog. Ser. 250, 117-124. (doi:10.3354/meps250117)
19. Goulet, T. L., LaJeunesse, T. C. & Fabricius, K. 2008 Symbiont specificity and bleaching susceptibility among soft corals during the 1998 GBR mass coral bleaching event. Mar. Biol. 154, 795-804. (doi:10.1007/s00227-008- 0972-5)
20. Hoegh-Guldberg, O. 1999 Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50, 839-866. (doi:10.1071/ MF99078)
21. Hoegh-Guldberg, O., Fine, M., Skirving, W., Johnstone, R., Dove, S. & Strong, A. 2005 Coral bleaching following wintry weather. Limnol. Oceanogr. 50, 265-271.
22. Hoegh-Guldberg, O. et al. 2007 Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742. (doi:10.1126/science.1152509)
23. Hughes, T. P. et al. 2003 Climate change, human impacts, and the resilience of coral reefs. Science 301, 929-933. (doi:10.1126/science.1085046) (Pubitemid 36994796)
24. Iglesias-Prieto, R. & Trench, R. K. 1997 Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar. Biol. 130, 23-33. (doi:10. 1007/s002270050221) (Pubitemid 28084499)
25. IPCC 2007 Climate change synthesis report. Contribution of working groups I, II, and III to the fourth assessment of the Intergovernmental Panel on Climate Change (eds R. Pachauri & A. Reisinger) pp. 104. Geneva.
26. Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. 2008 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. (doi:10.1098/rspb. 2008.0069) (Pubitemid 351653015)
27. LaJeunesse, T. C. 2002 Community structure and diversity of symbiotic dinoflagellate populations from a Caribbean coral reef. Mar. Biol. 141, 387-400.
28. LaJeunesse, T. C. 2005 'Species' radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol. 22, 570-581. (doi:10.1093/molbev/msi042) (Pubitemid 40299506)
29. LaJeunesse, T. C. & Pinzón, J. 2007 Screening intragenomic rDNA for dominant variants can provide a consistent retrieval of evolutionary persistent ITS (rDNA) sequences. Mol. Phylogenet. Evol. 45, 417-422. (doi:10. 1016/j.ympev.2007.06.017)
30. LaJeunesse, T. C. & Trench, R. K. 2000 The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal anemone, Anthopleura elegantissima (Brandt). Biol. Bull. 199, 126-134.
31. LaJeunesse, T. C., Bhagooli, R., Hidaka, M., deVantier, L., Done, T. J., Schmidt, G. W., Fitt, W. K. & Hoegh-Guldberg, O. 2004 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. (doi:10. 3354/meps284147)
32. LaJeunesse, T. C., Lee, S., Bush, S. & Bruno, J. F. 2005 Persistence of non-Caribbean algal symbionts in Indo-Pacific mushroom corals released to Jamaica 35 years ago. Coral Reefs 24, 157-159. (doi:10.1007/ s00338-004-0436-4)
33. LaJeunesse, T. C., Reyes-Bonilla, H., Warner, M. E., Wills, M., Schmidt, G. W. & Fitt, W. K. 2008 Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol. Oceanogr. 53, 719-727.
34. LaJeunesse, T. C., Finney, J. C., Smith, R. T. & Oxenford, H. 2009 Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc. R. Soc. B 276, 4139-4148. (doi:10.1098/rspb.2009.1405)
35. LaJeunesse, T. C., Pettay, D. T., Sampayo, E. M., Phongsuwan, N., Brown, B., Obura, D., Hoegh-Guldberg, O. & Fitt, W. K. 2010 Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr. 37, 785-800.
36. Lewis, C. L. & Coffroth, M. A. 2004 The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304, 1490-1492. (doi:10.1126/science. 1097323) (Pubitemid 38720926)
37. Loh, W. K. W., Loi, T., Carter, D. & Hoegh-Guldberg, O. 2001 Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar. Ecol. Prog. Ser. 222, 97-107. (doi:10.3354/meps222097)
38. Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H. & van Woesik, R. 2001 Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122-131. (doi:10.1046/j.1461-0248. 2001.00203.x) (Pubitemid 32228508)
39. Maynard, J., Baird, A. H. & Pratchett, M. 2008 Revisiting the Cassandra syndrome; the changing climate of coral reef research. Coral Reefs 27, 745-749. (doi:10.1007/ s00338-008-0432-1)
40. Mostafavi, P. G., Fatemi, S. M. R., Shahhosseiny, M. H., Hoegh-Guldberg, O. & Loh, W. K. W. 2007 Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Mar. Biol. 153, 25-34.
41. Pettay, D. T. & LaJeunesse, T. C. 2007 Microsatellites from clade B Symbiodinium spp. specialized for Caribbean corals in the genus Madracis. Mol. Ecol. Notes 7, 1271-1274. (doi:10.1111/j.1471-8286.2007.01852.x) (Pubitemid 350059248)
42. Pettay, D. T. & LaJeunesse, T. C. 2009 Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in 'stress-tolerant' clade D Symbiodinium. Mol. Ecol. Res. 9, 1022-1025.
43. Reyes-Bonilla, H. 2001 Effects of the 1997-1998 El Niño-Southern Oscillation on coral communities of the Gulf of California. Bull. Mar. Sci. 69, 251-266.
44. Reyes-Bonilla, H., Carriquiry, J. D., Leyte Morales, G. E. & Cupul Magana, A. L. 2002 Effects of the El Niño-Southern Oscillation and the anti-El Niño event (1997-1999) on coral reefs of the western coast of México. Coral Reefs 21, 368-372.
45. Rowan, R. 2004 Thermal adaptation in reef coral symbionts. Nature 430, 742. (doi:10.1038/430742a) (Pubitemid 39071338)
46. Rowan, R. & Powers, D. A. 1991 Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65-73. (doi:10.3354/meps071065)
47. Rowan, R., Knowlton, N., Baker, A. & Jara, J. 1997 Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265-269. (doi:10.1038/40843) (Pubitemid 27317968)
48. Sampayo, E. M., Ridgeway, T., Bongaerts, P. & Hoegh-Gulberg, O. 2008 Bleaching susceptibility and mortality of corals are determined by fine-scale differences in sym-biont type. Proc. Natl Acad. Sci. 105, 10 444-10 449. (doi:10.1073/pnas.0708049105)
49. Sampayo, E., Dove, S. & LaJeunesse, T. C. 2009 Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol. Ecol. 18, 500-519. (doi:10.1111/j.1365-294X.2008.04037.x)
50. Santos, S. R., Shearer, T. L., Hannes, A. R. & Coffroth, M. A. 2004 Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol. Ecol. 13, 459-469. (doi:10.1046/j.1365-294X.2003.02058.x) (Pubitemid 38143387)
51. Schoenberg, D. A. & Trench, R. K. 1980 Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal, and specificity in its symbioses with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc. R. Soc. Lond. B 207, 445-460. (doi:10.1098/rspb.1980.0033)
52. Seutin, G., White, B. N. & Boag, P. T. 1991 Preservation of avian blood and tissue samples for DNA analyses. Can. J. Zool. 69, 82-92. (doi:10.1139/z91-013)
53. Stat, M., Loh, W. K. W., Hoegh-Guldberg, O. & Carter, D. A. 2008 Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27, 763-772. (doi:10.1007/s00338-008-0412-5)
54. Stat, M., Loh, W. K. W., LaJeunesse, T. C., Hoegh-Guld-berg, O. & Carter, D. A. 2009 Coral-endosymbiont stability following a natural bleaching event. Coral Reefs 28, 709-713.
55. Stimson, J. 1997 The annual cycle of density of zooxanthel-lae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 214, 35-48. (doi:10.1016/S0022-0981(96)02753-0) (Pubitemid 27265417)
56. Thornhill, D. J., Fitt, W. K. & Schmidt, G. W. 2006a Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25, 515-519. (doi:10.1007/s00338-006-0157-y) (Pubitemid 44748966)
57. Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. 2006b Multi-year seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711-722. (doi:10.1007/s00227-005-0114-2) (Pubitemid 43183831)
58. Thornhill, D., Xiang, Y., Fitt, W. K. & Santos, S. R. 2009 Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. Plos One 4, e6262.
59. Toller, W. W., Rowan, R. & Knowlton, N. 2001 Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol. Bull. 201, 360-373. (doi:10.2307/1543614)
60. van Oppen, M. J. H., Mahini, A. J. & Done, T. J. 2005 Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24, 482-487.
61. Veron, J. E. N. 2000 Corals of the world, pp. 1382. Townsville: Australian Institute of Marine Science.
62. Warner, M. E., Fitt, W. K. & Schmidt, G. W. 1996 The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 19, 291-299. (doi:10.1111/j.1365-3040. 1996.tb00251.x)
63. Warner, M. E., LaJeunesse, T. C., Robison, J. D. & Thur, R. M. 2006 The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol. Oceanogr. 51, 1887-1897.