The Occurrence of Mixed Infections of Symbiodinium (Dinoflagellata) within Individual Hosts

Journal of Phycology

Volumn 48, Issue 6, 2012, Pages 1306-1316

  Fay, Scott A ^a   Weber, Michele X ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Coral; Dinoflagellate; Ecology; Mixed infection; Mutualism; Shuffling; Switching; Symbiodinium; Symbiosis

Indexed keywords

ACROPORA; ALGAE; ANTHOZOA; CNIDARIA; DINOPHYCEAE; FORAMINIFERA; MOLLUSCA; MONTASTRAEA; POCILLOPORA; PORITES; SCLERACTINIA; SYMBIODINIUM;

EID: 84870905518     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01220.x     Document Type: Short Survey

References (126)

1. Abrego, D., van Oppen, M. J. H. & Willis, B. L. 2009a. Highly infectious symbiont dominates initial uptake in coral juveniles. Mol. Ecol. 18:3518-31.
2. Abrego, D., van Oppen, M. J. H. & Willis, B. L. 2009b. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol. Ecol. 18:3532-43.
3. Apprill, A. M. & Gates, R. D. 2007. Recognizing diversity in coral symbiotic dinoflagellate communities. Mol. Ecol. 16:1127-34.
4. Baillie, B. K., Belda-Baillie, C. A. & Maruyama, T. 2000. Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J. Phycol. 36:1153-61.
5. Baird, A. H., Cumbo, V. R., Leggat, W. & Rodriguez-Lanetty, M. 2007. Fidelity and flexibility in coral symbioses. Mar. Ecol. Prog. Ser. 347:307-9.
6. Baker, A. C. 1999. The symbiosis ecology of reef-building corals. PhD Dissertation, University of Miami, Miami. 120pp.
7. Baker, A. C. 2001. Reef corals bleach to survive change. Nature 411:765-6.
8. Baker, A. C. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Syst. 34:661-89.
9. Baker, A. C. & Romanski, A. M. 2007. Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Mar. Ecol. Prog. Ser. 335:237-42.
10. Banaszak, A. T., LaJeunesse, T. C. & Trench, R. K. 2000. The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 249:219-33.
11. Barneah, O., Brickner, I., Hooge, M., Weis, V. M., LaJeunesse, T. C. & Benayahu, Y. 2007. Three party symbiosis: acoelomorph worms, corals and unicellular algal symbionts in Eilat (Red Sea). Mar. Biol. 151:1215-23.
12. Belda-Baillie, C. A., Sison, M., Silvestre, V., Villamor, K., Monje, V., Gomez, E. D. & Baillie, B. K. 1999. Evidence for changing symbiotic algae in juvenile tridacnids. J. Exp. Mar. Biol. Ecol. 241:207-21.
13. Berkelmans, R. & van Oppen, M. J. H. 2006. 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. B: Biol. Sci. 273:2305-12.
14. Bever, J. D. 2002. Negative feedback within a mutualism: host' specific growth of mycorrhizal fungi reduces plant benefit. Proc. R. Soc. B: Biol. Sci. 269:2595-601.
15. Bever, J. D., Richardson, S. C., Lawrence, B. M., Holmes, J. & Watson, M. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol. Lett. 12:13-21.
16. Carlos, A. A., Baillie, B. K. & Maruyama, T. 2000. Diversity of dinoflagellate symbionts (zooxanthellae) in a host individual. Mar. Ecol. Prog. Ser. 195:93-100.
17. Chen, C. A., Wang, A. T., Fang, L. S. & Yang, Y. W. 2005a. Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar. Ecol. Prog. Ser. 295:113-21.
18. Chen, C. A., Yang, Y.-W., Wei, N. V., Tsai, W.-S. & Fang, L.-S. 2005b. Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24:11-22.
19. Coffroth, M. A., Poland, D. M., Petrou, E. L., Brazeau, D. A. & Holmberg, J. C. 2010. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS ONE 5:e13258.
20. Coffroth, M. A. & Santos, S. R. 2005. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19-34.
21. Coffroth, M. A., Santos, S. R. & Goulet, T. L. 2001. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar. Ecol. Prog. Ser. 222:85-96.
22. Correa, A. M. S. & Baker, A. C. 2009. Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81-93.
23. Correa, A. M. S. & Baker, A. C. 2011. Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob. Change Biol. 17:68-75.
24. th. International Society for Reef Studies, Ft. Lauderdale Florida.
25. Correa, A. M. S., Brandt, M. E., Smith, T. B., Thornhill, D. J. & Baker, A. C. 2009a. Symbiodinium associations with diseased and healthy scleractinian corals. Coral Reefs 28:437-48.
26. Correa, A. M. S., McDonald, M. D. & Baker, A. C. 2009b. Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar. Biol. 156:2403-11.
27. Crabbe, M. J. C. & Carlin, J. P. 2009. Multiple Symbiodinium clades in Acropora species scleractinian corals from the Ningaloo reef, Australia. Int. J. Integr. Biol. 5:72-4.
28. Darius, H. T., Dauga, C., Grimont, P. A. D., Chungue, E. & Martin, P. M. V. 1998. Diversity in symbiotic dinoflagellates (pyrrhophyta) from seven scleractinian coral species: restriction enzyme analysis of small subunit ribosomal RNA genes. J. Eukaryotic Microbiol. 45:619-27.
29. DeSalvo, M. K., Sunagawa, S., Fisher, P. L., Voolstra, C. R., Iglesias-Prieto, R. & Medina, M. 2010. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol. Ecol., 19:1174-86.
30. Diekmann, O. E., Bak, R. P. M., Tonk, L., Stam, W. T. & Olsen, J. L. 2002. No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef. Mar. Ecol. Prog. Ser. 227:221-32.
31. Dong, Z. J., Huang, H., Huang, L. M. & Li, Y. C. 2009. Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the Xisha Islands in the South China Sea. J. Syst. Evol. 47:321-6.
32. Dong, Z., Huang, H., Huang, L., Li, Y. & Li, X. 2008. PCR-RFLP analysis of large subunit rDNA of symbiotic dinoflagellates in scleractinian corals from Luhuitou fringing reef of Sanya, Hainan. Shengwu Duoyangxing. 16:498-502.
33. Douglas, A. E. 1998. Host benefit and the evolution of specialization in symbiosis. Heredity 81:599-603.
34. Douglas, A. E. 1994. Symbiotic Interactions, Oxford University Press, USA.
35. Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, M. J. H. 2004. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13:2445-58.
36. Fay, S., Weber, M. & Lipps, J. 2009. The distribution of Symbiodinium diversity within individual host foraminifera. Coral Reefs 28:717-26.
37. Finney, J. C., Pettay, D. T., Sampayo, E. M., Warner, M. E., Oxenford, H. A. & LaJeunesse, T. C. 2010. The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microbial Ecol. 60:250-63.
38. Frade, P. R., de Jongh, F., Vermeulen, F., van Bleijswijk, J. & Bak, R. P. M. 2008. Variation in symbiont distribution between closely related coral species over large depth ranges. Mol. Ecol. 17:691-703.
39. Frank, S. A. 1996. Host-symbiont conflict over the mixing of symbiotic lineages. Proc. R. Soc. B: Biol. Sci. 263:339-44.
40. Garren, M., Walsh, S. M., Caccone, A. & Knowlton, N. 2006. Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25:503-12.
41. Goulet, T. L. 2006. Most corals may not change their symbionts. Mar. Ecol. Prog. Ser. 321:1-7.
42. Goulet, T. L. 2007. Most scleractinian corals and octocorals host a single symbiotic zooxanthella clade. Mar. Ecol. Prog. Ser. 335:243-8.
43. Goulet, T. L. & Coffroth, M. A. 2003. Genetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on small subunit rDNA and multilocus DNA fingerprinting. Mar. Biol. 142:233-9.
44. Hannes, A. R., Barbeitos, M. & Coffroth, M. A. 2009. Stability of symbiotic dinoflagellate type in the octocoral Briareum asbestinum. Mar. Ecol. Prog. Ser. 391:65-72.
45. Harii, S., Yasuda, N., Rodriguez-Lanetty, M., Irie, T. & Hidaka, M. 2009. Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals. Mar. Biol. 156:1203-12.
46. Heath, K. D. & Tiffin, P. 2009. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 63:652-62.
47. Hill, M., Allenby, A., Ramsby, R., Schönberg, C. & Hill, A. 2011. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol. Phylogenet. Evol. 59:81-8. doi:10.1016/j.ympev.2011.01.006
48. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D. et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-42.
49. Huang, H., Dong, Z.-J., Huang, L.-M. & Zhang, J.-B. 2006. Restriction fragment length polymorphism analysis of large subunit rDNA of symbiotic dinoflagellates from scleractinian corals in the Zhubi Coral Reef of the Nansha Islands. J. Integr. Plant Biol. 48:148-52.
50. Hunter, R. L., LaJeunesse, T. C. & Santos, S. R. 2007. Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J. Phycol. 43:120-8.
51. 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.
52. Kemp, D. W., Cook, C. B., LaJeunesse, T. C. & Brooks, W. R. 2006. A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida. J. Exp. Mar. Biol. Ecol. 335:266-76.
53. Kemp, D. W., Fitt, W. K. & Schmidt, G. W. 2008. A microsampling method for genotyping coral symbionts. Coral Reefs 27:289-93.
54. Kerr, A. M. T. 2005. Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biol. Rev. Camb. Philos. Soc. 80:543-58.
55. LaJeunesse, T. C. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141:387-400.
56. LaJeunesse, T. C., Bhagooli, R., Hidaka, M., DeVantier, L., Done, T., 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. 284:147-61.
57. LaJeunesse, T. C., Bonilla, H. R., 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. 53:719-27.
58. LaJeunesse, T. C., Loh, W. K. W., van Woesik, R., Hoegh-Guldberg, O., Schmidt, G. W. & Fitt, W. K. 2003. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48:2046-54.
59. LaJeunesse, T. C., Smith, R. T., Finney, J. & Oxenford, H. 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral "bleaching" event. Proc. R. Soc. B: Biol. Sci. 276:4139-48.
60. LaJeunesse, T. C., Smith, R., Walther, M., Pinzón, J., Pettay, D. T., McGinley, M., Aschaffenburg, M. et al. 2010. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc. R. Soc. B: Biol. Sci. 277:2925-34.
61. LaJeunesse, T. C. & Thornhill, D. J. 2011. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolutionary history through psbA non-coding region genotyping. PLoS ONE 6:e29103.
62. LaJeunesse, T. C. & Trench, R. K. 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol. Bull. Woods Hole, Massachusetts 199:126-34.
63. Lewis, L. A. & Muller-Parker, G. 2004. Phylogenetic placement of "zoochlorellae" (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima. Biol. Bull. Woods Hole, Massachusetts 207:87-92.
64. Lien, Y.-T., Nakano, Y., Plathong, S., Fukami, H., Wang, J.-T. & Chen, C. A. 2007. Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26:35-44.
65. Little, A. F., van Oppen, M. J. H. & Willis, B. L. 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492-4.
66. Loh, W. K. W., Cowlishaw, M. & Wilson, N. G. 2006. Diversity of Symbiodinium dinoflagellate symbionts from the Indo-Pacific sea slug Pteraeolidia ianthina (Gastropoda: Mollusca). Mar. Ecol. Prog. Ser. 320:177-84.
67. Loram, J. E., Boonham, N., O'Toole, P., Trapido-Rosenthal, H. G. & Douglas, A. E. 2007a. Molecular quantification of symbiotic dinoflagellate algae of the genus Symbiodinium. Biol. Bull. Woods Hole, Massachusetts 212:259-68.
68. Loram, J. E., Trapido-Rosenthal, H. G. & Douglas, A. E. 2007b. Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol. Ecol. 16:4849-57.
69. Magalon, H., Baudry, E., Huste, A., Adjeroud, M. & Veuille, M. 2006. High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific. Mar. Biol. 148:913-22.
70. Magalon, H., Flot, J. F. & Baudry, E. 2007. Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551-8.
71. McClanahan, T. R., Maina, J., Moothien-Pillay, R. & Baker, A. C. 2005. Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. Mar. Ecol. Prog. Ser. 298:131-42.
72. McCutcheon, J. P., McDonald, B. R. & Moran, N. A. 2009. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. USA 106:15394-9.
73. McCutcheon, J. P. & Moran, N. A. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. USA 104:19392-7.
74. Medina, M. & Sachs, J. L. 2010. Symbiont genomics, our new tangled bank. Genomics 95:129-37.
75. Messenger, S. L., Molineux, I. J. & Bull, J. J. 1999. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. B: Biol. Sci. 266:397-404.
76. Mieog, J. C., van Oppen, M. J. H., Berkelmans, R., Stam, W. T. & Olsen, J. L. 2009. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol. Ecol. Resources 9:74-82.
77. Mieog, J. C., van Oppen, M. J. H., Cantin, N. E., Stam, W. T. & Olsen, J. L. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449-57.
78. Oliver, K. M., Moran, N. A. & Hunter, M. S. 2006. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B: Biol. Sci. 273:1273-80.
79. Oliver, T. A. & Palumbi, S. R. 2009. Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar. Ecol. Prog. Ser. 378:93-103.
80. van Oppen, M. J. H. 2004. Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar. Biol. 144:1-7.
81. van Oppen, M. J. H., Palstra, F. P., Piquet, A. M. T. & Miller, D. J. 2001. Patterns of coral-dinoflagellate associations in Acropora: Significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc. R. Soc. B: Biol. Sci.268:1759-67.
82. Pochon, X., Garcia -Cuetos, L., Baker, A. C., Castella, E. & Pawlowski, J. 2007. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867-82.
83. Pochon, X. & Gates, R. D. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol. Phylogenet. Evol. 56:492-7.
84. Pochon, X., Montoya-Burgos, J. I., Stadelmann, B. & Pawlowski, J. 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phylogenet. Evol. 38:20-30.
85. Pochon, X., Stat, M., Takabayashi, M., Chasqui, L., Chauka, L. J., Logan, D. D. K. & Gates, R. D. 2010. Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a hawaiian reef environment. J. Phycol. 46:53-65.
86. Poulsen, M. & Boomsma, J. J. 2005. Mutualistic fungi control crop diversity in fungus-growing ants. Science 307:741-4.
87. Poulsen, M., Fernandez-Marin, H., Currie, C. R. & Boomsma, J. J. 2009. Ephemeral windows of opportunity for horizontal transmission of fungal symbionts in leaf-cutting ants. Evolution 63:2235-47.
88. Robison, J. D. & Warner, M. E. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42:568-79.
89. Rodriguez-Lanetty, M., Chat, H. R. & Song, I. 2000. Genetic diversity of symbiotic dinoflagellates associated with anthozoans from Korean waters. Proc. Int. Symp. Coral Reefs, 9th. International Society for Reef Studies, Bali.
90. Rodriguez-Lanetty, M., Loh, W., Carter, D. & Hoegh-Guldberg, O. 2001. Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar. Biol. (Berlin) 138:1175-181.
91. Rowan, R. & Knowlton, N. 1995. Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl. Acad. Sci. USA 92:2850-3.
92. Rowan, R., Knowlton, N., Baker, A. & Jara, J. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265-9.
93. Rowan, R. & Powers, D. A. 1991. Molecular genetic identification of symbiotic dinoflagellates zooxanthellae. Mar. Ecol. Prog. Ser. 71:65-73.
94. Sachs, J. L. & Simms, E. L. 2008. The origins of uncooperative rhizobia. Oikos 117:961-6.
95. Sachs, J. L. & Wilcox, T. P. 2006. A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc. R. Soc. B: Biol. Sci. 273:425-9.
96. Sampayo, E. M., Dove, S. & Lajeunesse, T. C. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol. Ecol. 18:500-19.
97. Sampayo, E. M., Franceschinis, L., Hoegh-Guldberg, O. & Dove, S. 2007. Niche partitioning of closely related symbiotic dinoflagellates. Mol. Ecol. 16:3721-33.
98. Santos, S. R. & Coffroth, M. A. 2003. Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium freudenthal are haploid. Biol. Bull. Woods Hole, Massachusetts 204:10-20.
99. Santos, S. R., Gutierrez-Rodriguez, C., Lasker, H. R. & Coffroth, M. A. 2003. Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Mar. Biol. 143:111-20.
100. 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. 13:459-69.
101. Savage, A. M., Goodson, M. S., Visram, S., Trapido-Rosenthal, H., Wiedenmann, J. & Douglas, A. E. 2002. Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar. Ecol. Prog. Ser. 244:17-26.
102. Schlick-Steiner, B. C., Steiner, F. M., Konrad, H., Seifert, B., Christian, E., Moder, K., Stauffer, C. & Crozier, R. H. 2008. Specificity and transmission mosaic of ant nest-wall fungi. Proc. Natl. Acad. Sci. USA 105:940-3.
103. Sebastian, C. R., Sink, K. J., McClanahan, T. R. & Cowan, D. A. 2009. Bleaching response of corals and their Symbiodinium communities in southern Africa. Mar. Biol. 156:2049-62.
104. Shaked, Y. & de Vargas, C. 2006. Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Mar. Ecol. Prog. Ser. 325:59-71.
105. Silverstein, R. N., Correa, A. M. S., LaJeunesse, T. C. & Baker, A. C. 2011. Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar. Ecol. Prog. Ser. 422:63-75.
106. Stat, M., Bird, C. E., Pochon, X., Chasqui, L., Chauka, L. J., Concepcion, G. T., Logan, D., Takabayashi, M., Toonen, R. J. & Gates, R. D. 2011. Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS ONE, 6:e15854.
107. Stat, M., Loh, W. K. W., Hoegh-Guldberg, O. & Carter, D. A. 2008a. Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27:763-72.
108. Stat, M., Loh, W., LaJeunesse, T., Hoegh-Guldberg, O. & Carter, D. 2009a. Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709-13.
109. Stat, M., Morris, E. & Gates, R. D. 2008b. Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl. Acad. Sci. USA 105:9256-61.
110. Stat, M., Pochon, X., Cowie, R. O. M. & Gates, R. D. 2009b. Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar. Ecol. Prog. Ser. 386:83-96.
111. Takahashi, S., Whitney, S. M. & Badger, M. R. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl. Acad. Sci. USA 106:3237-42.
112. Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. 2006. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148:711-22.
113. Thornhill, D. J., Lajeunesse, T. C. & Santos, S. R. 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol. Ecol. 16:5326-40.
114. Toller, W. W., Rowan, R. & Knowlton, N. 2001a. Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol. Bull. Woods Hole, Massachusetts 201:360-73.
115. Toller, W. W., Rowan, R. & Knowlton, N. 2001b. Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol. Bull. Woods Hole, Massachusetts 201:348-59.
116. Ulstrup, K. E. & van Oppen, M. J. H. 2003. Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol. Ecol. 12:3477-84.
117. Ulstrup, K. E., van Oppen, M. J. H., Kuehl, M. & Ralph, P. J. 2007. Inter-polyp genetic and physiological characterisation of Symbiodinium in an Acropora valida colony. Mar. Biol. 153:225-34.
118. Venera-Ponton, D. E., Diaz-Pulido, G., Rodriguez-Lanetty, M. & Hoegh-Guldberg, O. 2010. Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs 29:1049-60.
119. Venn, A. A., Loram, J. E., Trapido-Rosenthal, H. G., Joyce, D. A. & Douglas, A. E. 2008. Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea. Biol. Bull. Woods Hole, Massachusetts 215:243-52.
120. Venn, A., Weber, F., Loram, J. & Jones, R. 2009. Deep zooxanthellate corals at the high latitude Bermuda Seamount. Coral Reefs 28:135-35.
121. Visram, S. & Douglas, A. E. 2006. Molecular diversity of symbiotic algae (zooxanthellae) in scleractinian corals of Kenya. Coral Reefs 25:172-6.
122. Wagner, D., Pochon, X., Irwin, L., Toonen, R. J. & Gates, R. D. 2010. Azooxanthellate? Most Hawaiian black corals contain Symbiodinium. Proc. R. Soc. B: Biol. Sci. 278:1323-8.
123. Warnecke, F., Luginbuehl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T., Cayouette, M. et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560-5.
124. Weis, V. M. 2008. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. l Exp. Biol. 211:3059-66.
125. Wier, A., Dolan, M., Grimaldi, D., Guerrero, R., Wagensberg, J. & Margulis, L. 2002. Spirochete and protist symbionts of a termite (Mastotermes electrodominicus) in Miocene amber. Proc. Natl. Acad. Sci. USA 99:1410-3.
126. Wood-Charlson, E. M., Hollingsworth, L. L., Krupp, D. A. & Weis, V. M. 2006. Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell. Microbiol. 8:1985-93.