The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium

Microbial Ecology

Volumn 60, Issue 1, 2010, Pages 250-263

  Finney, J Christine ^a   Pettay, Daniel Tye ^b   Sampayo, Eugenia M ^b   Warner, Mark E ^c   Oxenford, Hazel A ^a   LaJeunesse, Todd C ^b  

^a UNIVERSITY OF THE WEST INDIES   (Jamaica)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA; RIBOSOMAL SPACER DNA;

ANIMAL; ANTHOZOA; ARTICLE; CENTRAL AMERICA; CLASSIFICATION; DINOFLAGELLATE; DNA SEQUENCE; ECOSYSTEM; GENETICS; GEOGRAPHY; MICROBIOLOGY; PHYLOGENY; SPECIES DIFFERENCE; SYMBIOSIS; CARIBBEAN;

ANIMALS; ANTHOZOA; CARIBBEAN REGION; DINOFLAGELLIDA; DNA, RIBOSOMAL SPACER; ECOSYSTEM; GEOGRAPHY; MICROSATELLITE REPEATS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

ANTHOZOA; CNIDARIA; COELENTERATA; DINOPHYCEAE; EUKARYOTA; SYMBIODINIUM;

EID: 77955419055     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-010-9681-y     Document Type: Article

References (66)

1. Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21: 409-421.
2. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioSci 27: 454-460.
3. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26: 601-611.
4. Berkelmans R, van Oppen MJH (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 Lond B 273: 2305-2312.
5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34: 661-689.
6. LaJeunesse TC (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22: 570-581.
7. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (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.
8. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251: 1348-1351.
9. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
10. Loh WK, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of thesymbiotic dinoflagellates from the wide ranging coral species Seriatopora hystix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser 222: 97-107.
11. Rodriguez-Lanetty M, Krupp D, Weis VM (2004) Distinct ITS types of Symbiodinium in clade C correlate to cnidarian/dinoflagellate specificity during symbiosis onset. Mar Ecol Prog Ser 275: 97-102.
12. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci USA 92: 2850-2853.
13. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of symbiotic dinoflagellates. Mol Ecol 16: 3721-3733.
14. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern great barrier reef corals relative to those of the Caribbean. Limnol Oceanogr 48: 2046-2054.
15. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-symbioses, diversity, and the effect of climate change. Pers Plant Ecol Evol Syst 8: 23-43.
16. Fukami H, Budd A, Paulay G, Sole-Cava A, Chen CA, Iwao K, Knowlton N (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427: 832-835.
17. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301: 958-960.
18. LaJeunesse TC, Thornhill DJ, Cox E, Stanton F, Fitt WK, Schmidt GW (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23: 596-603.
19. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. Proc Int Coral Reef Symp 8th Panama 2: 1295-1300.
20. Diekmann OE, Olsen JL, Stam WT, Bak RPM (2003) Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22: 29-33.
21. Santos SR, Shearer TL, Hannes AR, Coffroth MA (2004) Fine scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyta) of the Caribbean. Mol Ecol 13: 459-469.
22. Thornhill DJ, Fitt WK, Schmidt GW (2006) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25: 515-519.
23. Thornhill D, LaJeunesse TC, Kemp DW, Fitt WKW, Schmidt GW (2006) Multi-year seasonal genotypic surveys of coral-algal symbiosis reveal prevalent stability or post-bleaching reversion. Mar Biol 148: 711-722.
24. Correa AMS, Brandt ME, Smith TB, Thronhill DJ, Baker AC (2009) Symbiodinium associations with diseased and healthy scleractinian corals. Coral Reefs 28: 437-448.
25. Frade PR, Bongaerts P, Wilkelhagen AJS, Tonk L, Bak RPM (2008) In situ photobiology of corals over large dept ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53: 2711-2723.
26. Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern Pacific. Proc 8th Int Coral Reef Symp 2: 1301-1306.
27. Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23: 465-472.
28. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, 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.
29. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New York.
30. Sampayo E, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18: 500-519.
31. Thornhill DJ, LaJeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16: 5326-5340.
32. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69: 82-92.
33. Pochon X, Garcia-Cuestos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in sorited foraminifera. Coral Reefs 26: 867-882.
34. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Gulberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105: 10444-10449.
35. LaJeunesse TC, Trench RK (2000) The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal anemone, Anthopleura elegantissima (Brandt). Biol Bull 199: 126-134.
36. Pettay DT, LaJeunesse TC (2007) Microsatellites from clade B Symbiodinium spp. specialized for Caribbean corals in the genus Madracis. Mol Ecol Notes 7: 1271-1274.
37. Swofford DL (2000) PAUP*, Phylogenetic analysis using parsimony (*and other methods), Version 4. 0b10. Sunderland, Mass, Sinauer.
38. Quinn JP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK.
39. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56: 879-886.
40. LaJeunesse TC, Pinzón JH (2007) Screening intragenomic rDNA for dominant variants can provide a consistent retrieval of evolutionarily persistent ITS (rDNA) sequences. Mol Phylogen Evol 45: 417-422.
41. LaJeunesse TC, Pinzón JH (2007) Screening intragenomic rDNA for dominant variants can provide a consistent retrieval of evolutionarily persistent ITS (rDNA) sequences. Mol Phyl Evol 45: 417-422.
42. Goulet TL, Coffroth MA (2003) Stability of an octocoral-algal symbiosis over time and space. Mar Ecol Prog Ser 250: 117-124.
43. Pettay DT, LaJeunesse TC (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.
44. Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204: 10-20.
45. Thornhill D, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 4: e6262.
46. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16: 372-380.
47. Baums I, Miller M, Hellberg M (2005) Regionally isolated populations of an imperilled Caribbean coral, Acropora palmata. Mol Ecol 14: 1377-1390.
48. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311: 522-527.
49. Budd A (2000) Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19: 25-35.
50. Barbrook AC, Visram S, Douglas AE, Howe CJ (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium. Protist 157: 159-171.
51. Moore RB, Ferguson KM, Loh WKW, Hoegh-Guldberg O, Carter DA (2003) Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Biol 53: 1725-1734.
52. LaJeunesse TC, Finney JC, Smith RT, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc Roy Soc Lond, B 276: 4139-4148.
53. Iglesias-Prieto R, Trench RK (1997) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. Proc 8th Int Coral Reef Symp 2: 1319-1324.
54. Banaszak AT, LaJeunesse TC, Trench RK (2000) Synthesis of MAA by symbiotic dinoflagellates in culture. J Exp Mar Biol Ecol 249: 219-233.
55. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways is symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105: 13674-13678.
56. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrohphyta). J Phycol 42: 568-579.
57. Iglesias-Prieto R, Trench RK (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.
58. Savage AM, Trapido-Rosenthal H, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244: 27-37.
59. Tchernov D, Gorbunov MY, de Vargas C, Narayan C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101: 13531-13535.
60. Warner ME, LaJeunesse TC, Robison JE, Thur RM (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.
61. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific and the Red Sea. Mar Ecol Prog Ser 60: 185-203.
62. Goreau T (1959) The ecology of Jamaican coral reefs: species compostion and zonation. Ecology 40: 67-90.
63. Hoogenboom MO, Connolly SR, Anthony KRN (2009) Effects of photoacclimation on the light niche of corals: a process-based approach. Mar Biol 156: 2493-2503.
64. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals' adaptive response to climate change. Nature 430: 741.
65. Coffroth MA, Santos SR (2005) Invited review: genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156: 19-34.
66. Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium, Dinophyta). Mar Biol 146: 17-27.