Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Thornhill, Daniel J ^a,b   Xiang, Yu ^a   Fitt, William K ^c   Santos, Scott R ^a  

^a AUBURN UNIVERSITY   (United States)

^b BOWDOIN COLLEGE   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CORAL REEF; DENATURING GRADIENT GEL ELECTROPHORESIS; DINOFLAGELLATE; ENVIRONMENT; GENE AMPLIFICATION; GENE LOCUS; GENETIC VARIABILITY; GENOTYPE; HOST RANGE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISM COLONY; POLYMERASE CHAIN REACTION; SPECIES DIVERSITY; SYMBIOSIS; TIME; ANIMAL; ANTHOZOA; ECOLOGY; PARASITOLOGY; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SPECIES DIFFERENCE;

ANTHOZOA; DINOPHYCEAE; INVERTEBRATA; METAZOA; MONTASTRAEA FAVEOLATA; PROTISTA; SCLERACTINIA; SYMBIODINIUM;

ANIMALS; ANTHOZOA; DINOFLAGELLIDA; ECOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 67650676001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006262     Document Type: Article

References (75)

1. Cowen RK, Luiza KM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287: 857-859.
2. Bode M, Bode L, Armsworth PR (2006) Larval dispersal reveals regional sources and sinks in the Great Barrier Reef. Mar Ecol Prog Ser 308: 17-25.
3. Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 76: 2373-2391.
4. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299: 107-109.
5. Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149: 1247-1256.
6. Benzie JAH, Williams ST (1997) Genetic structure of giant clam ( Tridacna maxima) populations in the west Pacific is not consistent with dispersal by present-day ocean currents. Evolution 51: 768-783.
7. Richards VP, Thomas JD, Stanhope MJ, Shivji MS (2007) Genetic connectivity in the Florida reef system: comparative phylogeography of commensal invertebrates with contrasting reproductive strategies. Mol Ecol 16: 139-157.
8. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54: 1590-1605.
9. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150: 57-68.
10. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: Implications for the recovery of endangered reefs. J Hered 98: 40-50.
11. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: 454-460.
12. Hoegh-Guldburg O (1999) Climate change, coral bleaching, and the future of the world's coral reefs. Mar Freshw Res 50: 839-866.
13. Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates. pp 545.
14. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymniodinium) microadriaticum Freudenthal, and its specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc Lond B 207: 405-427.
15. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76: 219-229.
16. Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113: 163-175.
17. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251: 1348-1351.
18. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a 'species' level marker. J Phycol 37: 866-880.
19. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
20. van Oppen MJH, Palstra FP, Piquet AMT, Miller D (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond B 268: 1759-1767.
21. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156: 19-34.
22. Santos SR, Gutiérrez-Rodríguez C, Lasker HR, Coffroth MA (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: 111-120.
23. Kirk NL, Ward JR, Coffroth MA (2005) Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress. Biol Bull 209: 227-234.
24. Kirk NL, Andras JP, Harvell CD, Santos SR, Coffroth MA (2009) Population structure of Symbiodinium sp. associated with the common sea fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time. Mar Biol 156: 1609-1623.
25. Howells EJ, van Oppen MJH, Willis BL (2009) High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28: 215-225.
26. Magalon H, Baudry E, Husté 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: 913-922.
27. Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar Ecol Prog Ser 74: 13-25.
28. 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.
29. Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraea annularis species complex: Patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201: 348-359.
30. Garren M, Walsh SM, 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: 503-512.
31. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multiyear, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148: 711-722.
32. Kemp DW, Fitt WK, Schmidt GW (2008) A microsampling method for genotyping coral symbionts. Coral Reefs 27: 289-293.
33. Thornhill DJ, Fitt WK, Schmidt GW (2006) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25: 515-519.
34. Santos SR, Shearer TL, Hannes AR, Coffroth MA (2004) Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol Ecol 13: 459-469.
35. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef building corals and relation to coral bleaching. Limnol Oceanogr 45: 677-685.
36. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 60: 82-92.
37. Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18: 500-519.
38. Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204: 10-20.
39. 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.
40. Blank RJ (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Mar Biol 94: 143-155.
41. Pfiester LA, Anderson DM (1987) Dinoflagellate reproduction. In: Taylor FJR, ed. The biology of dinoflagellates. London: Blackwell. pp 611-648.
42. Andras JP, Kirk NL, Coffroth MA, Harvell CD (2009) Isolation and characterization of microsatellite loci in Symbiodinium B1/B184, the dinoflagellate symbiont of the Caribbean sea fan coral, Gorgonia ventalina. Mol Ecol Resour 9: 989-993.
43. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
44. Stat M, Loh WKW, Hoegh-Guldberg O, Carter D (2008) Host symbiont acquisition strategy drives Symbiodinium diversity in the southern Great Barrier Reef. Coral Reefs 27: 763-772.
45. Foster NL, Baums IB, Mumby PJ (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76: 384-391.
46. Yakovleva IM, Baird AH, Yamamoto HM, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378: 105-112.
47. Loeblich ARIII, Sherley JL (1979) Observations on the theca of the mobile phase of free-living and symbiotic isolates of Zooxanthella microadriaticum (Freudenthal) comb. nov. J Mar Biolog Assoc UK 59: 195-205.
48. Chang FH (1983) Winter phytoplankton and microzooplankton populations off the coast of Westland, New Zealand, 1979. N Z J Mar Freshwater Res 17: 279-304.
49. Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35: 1054-1062.
50. Gou WL, Sun J, Li XQ, Zhen Y, Xin Z, Yu ZG, Li RX (2003) Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P.R. China. J Exp Mar Biol Ecol 296: 135-144.
51. Santos SR (2004) Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P. R. China. J Phycol 40: 395-397.
52. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium (Freudenthal) can initiate symbioses with reef cnidarians. Curr Biol 16: R985-R987.
53. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53: 1853-1861.
54. Porto I, Granados C, Restrepo JC, Sánchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS One 3: e2160.
55. Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222: 85-96.
56. Thornhill DJ, Daniel MW, LaJeunesse TC, Fitt WK, Schmidt GW (2006) Natural infections of aposymbiotic Cassiopea xamachana from environmental pools of Symbiodinium. J Exp Mar Biol Ecol 338: 50-56.
57. Steele RD (1975) Stages in the life history of symbiotic zooxanthellae pellets extruded by its host Aiptasia tagetes (Duch. and Mich.) (Coelenterata, Anthozoa). Biol Bull 149: 590-600.
58. Steele RD (1977) The significance of zooxanthellae containing pellets extruded by sea anemones. Bull Mar Sci 27: 591-594.
59. Trench RK (1979) The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 330: 485-532.
60. Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle and morphology. J Protozool 9: 45-52.
61. Fitt WK, Trench RK (1983) The relation of diel patterns of cell division of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94: 421-432.
62. Muscatine L, Pool RR (1979) Regulation of numbers of intracellular algae. Proc R Soc Lond B 204: 131-139.
63. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153: 63-74.
64. Maruyama T, Heslinga GA (1997) Fecal discharge of zooxanthellae in the giant clam Tridacna derasa, with reference to their in situ growth rate. Mar Biol 127: 473-477.
65. Kinzie RA, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: Experimental test of critical assumptions. Biol Bull 200: 51-58.
66. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58: 324-337.
67. Budd AF, Pandolfi JM (2004) Overlapping species boundaries and hybridization within the Montastraea "annularis" reef coral complex in the Pleistocene of the Bahamas Islands. Paleobiology 30: 396-425.
68. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34: 661-689.
69. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (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: 449-457.
70. Lewis CL, Coffroth MA (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304: 1490-1492.
71. Carlon DB, Lippe C (2008) Fifteen new microsatellite markers for the reef coral Favia fragum and a new Symbiodinium microsatellite. Mol Ecol Resour 8: 870-873.
72. Fitt WK (1985) Effect of different strains of the zooxanthella Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts. Proc 5th Int Coral Reef Congr 6: 131-136.
73. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. BioScience 43: 320-326.
74. Baker AC (2001) Reef corals bleach to survive change. Nature 411: 765-766.
75. 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.