Marine Biology

, Volume 156, Issue 8, pp 1609–1623 | Cite as

Population structure of Symbiodinium sp. associated with the common sea fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time

  • Nathan L. Kirk
  • Jason P. Andras
  • C. Drew Harvell
  • Scott R. Santos
  • Mary Alice Coffroth
Original Paper

Abstract

Numerous marine invertebrates form endosymbiotic relationships with dinoflagellates in the genus Symbiodinium. However, few studies have examined the fine-scale population structure of these symbionts. Here, we describe the genetic structure of Symbiodinium type “B1/B184” inhabiting the gorgonian Gorgoniaventalina along the Florida Keys. Six polymorphic microsatellite loci were utilized to examine 16 populations along the Upper, Middle, and Lower Keys spanning a range of ~200 km. Multiple statistical tests detected significant differentiation in 54–92% of the 120 possible pairwise comparisons between localities, suggesting low levels of gene flow in these dinoflagellates. In general, populations clustered by geographic region and/or reefs in close proximity. Some of the sharpest population differentiation was detected between Symbiodinium from deep and shallow sites on the same reef. In spite of the high degree of population structure, alleles and genotypes were shared among localities, indicating some connectivity between Symbiodinium populations associated with G. ventalina.

Supplementary material

227_2009_1196_MOESM1_ESM.eps (324 kb)
Supplementary Fig. 1. Ln likelihood estimates [P(X|K)] for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes all sampling locations (EPS 323 kb)
227_2009_1196_MOESM2_ESM.eps (342 kb)
Supplementary Fig. 2. Delta K estimates for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes all sampling locations and was utilized to estimate the most likely number of population clusters as described in Evanno et al. (2005). (EPS 342 kb)
227_2009_1196_MOESM3_ESM.eps (317 kb)
Supplementary Fig. 3. Ln likelihood estimates [P(X|K)] for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes only shallow sampling locations. (EPS 317 kb)
227_2009_1196_MOESM4_ESM.eps (344 kb)
Supplementary Fig. 4. Delta K estimates for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes only shallow sampling locations and was utilized to estimate the most likely number of population clusters as described in Evanno et al. (2005). (EPS 344 kb)
227_2009_1196_MOESM5_ESM.eps (348 kb)
Supplementary Fig. 5. Ln likelihood estimates [P(X|K)] for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes only deep sampling locations. (EPS 348 kb)
227_2009_1196_MOESM6_ESM.eps (347 kb)
Supplementary Fig. 6. Delta K estimates for the number of population clusters (k) in Symbiodinium of Gorgonia ventalina from the Florida Keys. Analysis includes only deep sampling locations and was utilized to estimate the most likely number of population clusters as described in Evanno et al. (2005). (EPS 346 kb)
227_2009_1196_MOESM7_ESM.doc (301 kb)
Supplementary Table 1. Allele frequencies within and across 16 Symbiodinium populations of Gorgonia ventalina in the Florida Keys for six microsatellite loci (dinucleotides: CA6.38, Gv2, Gv42; trinucleotides: Gv100, Sym155, Sym254). Most frequent allele is denoted in bold. The number of samples with single and multiple alleles are presented for each locus. n= the total number of alleles recovered at each sample location, “1 allele” is the number of samples containing a single allele, “2 alleles” is the number of samples containing 2 alleles, and “3 alleles” is the number of samples with 3 alleles at a given locus. Site abbreviations are given in Table 1. (DOC 301 kb)
227_2009_1196_MOESM8_ESM.doc (559 kb)
Supplementary Table 2. Characteristics and distribution of the 388 genotypes identified from the Symbiodinium populations of Gorgonia ventalina in the Florida Keys. Genotypes are based on allele sizes (in bp) for six microsatellite loci. Genotype frequency by recovery location is denoted. Site abbreviations are given in Table 1 (DOC 559 kb)
227_2009_1196_MOESM9_ESM.doc (71 kb)
Supplementary Table 3. Bayesian analyses of the Symbiodinium populations of Gorgonia ventalina in the Florida Keys. a) Proportion of individuals from each site assigned to the two proposed populations (clusters) using a Bayesian clustering method of the original 16 sample populations. Bold indicates the cluster that a majority of the samples from the original populations belong to (i.e., the most probable cluster). b) Proportion of individuals from shallow sites only assigned into four proposed populations. c) Proportion of individuals from deep sites only assigned into two proposed populations (DOC 71 kb)

References

  1. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond B Biol Sci 275:2273–2282. doi:10.1098/rspb.2008.0180 CrossRefGoogle Scholar
  2. 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 Res. doi:10.1111/j.1755-0998.2009.02549.x
  3. Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:15–17. doi:10.1111/j.1471-8286.2006.01522.x CrossRefGoogle Scholar
  4. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766. doi:10.1038/35081151 PubMedCrossRefGoogle Scholar
  5. Baker AC (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 CrossRefGoogle Scholar
  6. Balloux F, Lehmann L, de Meeus T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:1635–1644PubMedGoogle Scholar
  7. 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. doi:10.1016/j.protis.2005.12.002 PubMedCrossRefGoogle Scholar
  8. Bayer FM (1961) The shallow-water Octocorallia of the West Indian region. Martinus Nijhoff, The HagueGoogle Scholar
  9. 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 Biol Sci 273:2305–2312. doi:10.1098/rspb.2006.3567 CrossRefGoogle Scholar
  10. Birkeland C (1974) The effect of wave action on the population dynamics of Gorgonia ventalina Linnaeus. In: Bayer FM (ed) Prostaglandins from Plexaura homomalla: ecology, utilization and conservation of a major medical marine resource. Studies in Tropical Oceanography, pp 115–126Google Scholar
  11. Blank RJ (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Mar Biol (Berl) 94:143–155. doi:10.1007/BF00392906 CrossRefGoogle Scholar
  12. Blank RJ, Huss VAR (1989) DNA divergency and speciation in Symbiodinium (Dinophyceae). Plant Syst Evol 163:153–163. doi:10.1007/BF00936511 CrossRefGoogle Scholar
  13. Blank RJ, Huss VAR, Kersten W (1988) Base composition of DNA from symbiotic dinoflagellates: a tool for phylogenetic classification. Arch Microbiol 149:515–520. doi:10.1007/BF00446754 CrossRefGoogle Scholar
  14. Boenigk J, Pfandl K, Garstecki T, Harms H, Novarino G, Chatzinotas A (2006) Evidence for geographic isolation and signs of endemism within a protistan morphospecies. Appl Environ Microbiol 72:5159–5164. doi:10.1128/AEM.00601-06 PubMedCrossRefGoogle Scholar
  15. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500. doi:10.1146/annurev.ecolsys.27.1.477 CrossRefGoogle Scholar
  16. Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (dinophyceae) isolates from tridacnids (bivalvia), cardids (bivalvia), a sponge (porifera), a soft coral (anthozoa), and a free-living strain. J Phycol 35:1054–1062. doi:10.1046/j.1529-8817.1999.3551054.x CrossRefGoogle Scholar
  17. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaption in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol (Berl) 76:219–229. doi:10.1007/BF00393021 CrossRefGoogle Scholar
  18. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34. doi:10.1016/j.protis.2005.02.004 PubMedCrossRefGoogle Scholar
  19. Coffroth MA, Lasker HR, Diamond ME, Bruenn JA, Bermingham E (1992) DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species. Mar Biol (Berl) 114:317–325. doi:10.1007/BF00349534 CrossRefGoogle Scholar
  20. Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96. doi:10.3354/meps222085 CrossRefGoogle Scholar
  21. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985–R987. doi:10.1016/j.cub.2006.10.049 PubMedCrossRefGoogle Scholar
  22. Colley NJ, Trench RK (1983) Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc R Soc Lond B Biol Sci 219:61–82. doi:10.1098/rspb.1983.0059 CrossRefGoogle Scholar
  23. DeWoody J, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957. doi:10.1111/j.1471-8286.2006.01449.x CrossRefGoogle Scholar
  24. Diekmann OE, Bak RPM, Tonk L, Stam WT, Olsen JL (2002) No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef. Mar Ecol Prog Ser 227:221–232. doi:10.3354/meps227221 CrossRefGoogle Scholar
  25. Dolan JR (2005) Biogeography of aquatic microbes. Aquat Microb Ecol 41:39–48. doi:10.3354/ame041039 CrossRefGoogle Scholar
  26. Dolan JR (2006) Microbial biogeography? J Biogeogr 33:199–200. doi:10.1111/j.1365-2699.2005.01406.x CrossRefGoogle Scholar
  27. Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Glob Change Biol 11:2251–2265. doi:10.1111/j.1365-2486.2005.01073.x CrossRefGoogle Scholar
  28. Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci USA 104:5483–5488. doi:10.1073/pnas.0610122104 PubMedCrossRefGoogle Scholar
  29. Edmunds PJ, Bruno JF, Carlon DB (2004) Effects of depth and microhabitat on growth and survivorship of juvenile corals in the Florida Keys. Mar Ecol Prog Ser 278:115–124. doi:10.3354/meps278115 CrossRefGoogle Scholar
  30. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. doi:10.1038/nrg1348 PubMedCrossRefGoogle Scholar
  31. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x PubMedCrossRefGoogle Scholar
  32. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variation inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  33. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  34. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  35. Fenchel T (2001) How dinoflagellates swim. Protist 152:329–338. doi:10.1078/1434-4610-00071 PubMedCrossRefGoogle Scholar
  36. Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784. doi:10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2 CrossRefGoogle Scholar
  37. Finlay BJ, Fenchel T (2004) Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist 155:237–244. doi:10.1078/143446104774199619 PubMedCrossRefGoogle Scholar
  38. Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae. Mar Biol (Berl) 81:9–17. doi:10.1007/BF00397620 CrossRefGoogle Scholar
  39. Fitt WK, Trench RK (1983) The relationship of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94:421–432. doi:10.1111/j.1469-8137.1983.tb03456.x CrossRefGoogle Scholar
  40. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45:111–136Google Scholar
  41. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008a) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53:2711–2723Google Scholar
  42. Frade PR, Englebert N, Faria J, Visser PM, Bak RPM (2008b) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27:913–925. doi:10.1007/s00338-008-0406-3 CrossRefGoogle Scholar
  43. Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J Protozool 9:45–52Google Scholar
  44. Glynn PW (1996) Coral reef bleaching: facts, hypotheses, and implications. Glob Change Biol 2:495–509. doi:10.1111/j.1365-2486.1996.tb00063.x CrossRefGoogle Scholar
  45. Goulet TL, Coffroth MA (2003) Stability of an octocoral-algal symbiosis over time and space. Mar Ecol Prog Ser 250:117–124. doi:10.3354/meps250117 CrossRefGoogle Scholar
  46. Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472Google Scholar
  47. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498Google Scholar
  48. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507. doi:10.1016/j.tree.2006.06.012 PubMedCrossRefGoogle Scholar
  49. Harada Y, Kawano S, Iwasa (1997) Probability of clonal identity: inferring the relative success of sexual versus clonal reproduction from spatial genetic patterns. J Ecol 85:591–600. doi:10.2307/2960530 CrossRefGoogle Scholar
  50. Hillebrand H, Watermann F, Karez R, Berninger U-G (2001) Differences in species richness patterns between unicellular and multicellular organisms. Oecologia 126:114–124. doi:10.1007/s004420000492 CrossRefGoogle Scholar
  51. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866. doi:10.1071/MF99078 CrossRefGoogle Scholar
  52. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez ED, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737. doi:10.1126/science.1152509 PubMedCrossRefGoogle Scholar
  53. Holsinger KE, Mason-Gamer RJ (1996) Hierarchical analysis of nucleotide diversity in geographically structured populations. Genetics 142:629–639PubMedGoogle Scholar
  54. 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. doi:10.1007/s00338-008-0450-z CrossRefGoogle Scholar
  55. Jokiel PL (1984) Long distance dispersal of reef corals by rafting. Coral Reefs 3:113–116. doi:10.1007/BF00263761 CrossRefGoogle Scholar
  56. Kinzie RA (1973) The zonation of West Indian gorgonians. Bull Mar Sci 23:93–155Google Scholar
  57. Kinzie RA (1974) Experimental infection of aposymbiotic gorgonian polyps with zooxanthellae. J Exp Mar Biol Ecol 15:335–345. doi:10.1016/0022-0981(74)90054-9 CrossRefGoogle Scholar
  58. Kinzie RA, Chee G (1979) The effect of different zooxanthellae on the growth of experimentally reinfected hosts. Biol Bull 156:315–327. doi:10.2307/1540920 PubMedCrossRefGoogle Scholar
  59. 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. doi:10.2307/3593112 PubMedCrossRefGoogle Scholar
  60. Kuguru B, Chadwick NE, Achituv Y, Zandbank K, Tchernov D (2008) Mechanisms of habitat segregation between corallimorpharians: photosynthetic parameters and Symbiodinium types. Mar Ecol Prog Ser 369:115–129. doi:10.3354/meps07651 CrossRefGoogle Scholar
  61. 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. doi:10.1046/j.1529-8817.2001.01031.x CrossRefGoogle Scholar
  62. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol (Berl) 141:387–400. doi:10.1007/s00227-002-0829-2 CrossRefGoogle Scholar
  63. Lampert-Karako S, Stambler N, Katcoff DJ, Achituv Y, Dubinsky Z, Simon-Blecher N (2008) Effects of depth and eutrophication on the zooxanthella clades of Stylophora pistillata from the Gulf of Eilat (Red Sea). Aquat Conserv Mar Freshw Ecosyst 18:1039–1045. doi:10.1002/aqc.927 CrossRefGoogle Scholar
  64. Lasker HR, Coffroth MA (1983) Octocoral distributions at Carrie Bow Cay, Belize. Mar Ecol Prog Ser 13:21–28. doi:10.3354/meps013021 CrossRefGoogle Scholar
  65. Lee TN, Smith N (2002) Volume transport variability through the Florida Keys tidal channels. Cont Shelf Res 22:1361–1377. doi:10.1016/S0278-4343(02)00003-1 CrossRefGoogle Scholar
  66. Lee TN, Williams E (1999) Mean distribution and seasonal variability of coastal currents and temperature in the Florida Keys with implications for larval recruitment. Bull Mar Sci 64:35–56Google Scholar
  67. Lee TN, Rooth C, Williams E, McGowan M, Szmant AM, Clarke ME (1992) Influence of Florida Current, gyres and wind-driven circulation on transport of larvae and recruitment in the Florida Keys coral reefs. Cont Shelf Res 12:971–1002. doi:10.1016/0278-4343(92)90055-O CrossRefGoogle Scholar
  68. Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores. Limnol Oceanogr 41:1490–1501Google Scholar
  69. Leichter JJ, Shellenbarger G, Genovese SJ, Wing SR (1998) Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Mar Ecol Prog Ser 166:83–97. doi:10.3354/meps166083 CrossRefGoogle Scholar
  70. Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407Google Scholar
  71. Littman RA, van Oppen MJH, Willis BL (2008) 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. doi:10.1016/j.jembe.2008.06.034 CrossRefGoogle Scholar
  72. 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 (Berl) 148:913–922. doi:10.1007/s00227-005-0133-z CrossRefGoogle Scholar
  73. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861Google Scholar
  74. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  75. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. doi:10.1038/nrmicro1341 PubMedCrossRefGoogle Scholar
  76. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064PubMedGoogle Scholar
  77. Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3Google Scholar
  78. Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia 41:56–70Google Scholar
  79. Moore RB, Ferguson KM, Loh WKW, Hoegh-Guldberg O, Carter D (2003) Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol 53:1725–1734. doi:10.1099/ijs.0.02594-0 PubMedCrossRefGoogle Scholar
  80. Muller-Parker G (1984) Dispersal of zooxanthellae on coral reefs by predators on cnidarians. Biol Bull 167:159. doi:10.2307/1541344 CrossRefGoogle Scholar
  81. Mundy C, Babcock R (2000) Are vertical distribution patterns of scleractinian corals maintained by pre- of post-settlement processes? A case study of three contrasting species. Mar Ecol Prog Ser 198:109–119. doi:10.3354/meps198109 CrossRefGoogle Scholar
  82. Nagai S, Lian C, Yamaguchi S, Hamaguchi M, Matsuyama Y, Itakura S, Shimada H, Kaga S, Yamauchi H, Sonda Y, Nishikawa T, Kim C-H, Hogetsu T (2007) Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters. J Phycol 43:43–54. doi:10.1111/j.1529-8817.2006.00304.x CrossRefGoogle Scholar
  83. Nagelkerken I, Buchan K, Smith GW, Bonair K, Bush P, Garzon-Ferreira J, Botero L, Gayle P, Harvell CD, Heberer C, Kim K, Petrovic C, Pors L, Yoshioka P (1997) Widespread disease in Caribbean sea fans: II. Patterns of infection and tissue loss. Mar Ecol Prog Ser 160:255–263. doi:10.3354/meps160255 CrossRefGoogle Scholar
  84. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292. doi:10.1086/282771 CrossRefGoogle Scholar
  85. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  86. Opresko DM (1973) Abundance and distribution of shallow-water gorgonians in the area of Miami, Florida. Bull Mar Sci 23:535–558Google Scholar
  87. Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118. doi:10.1016/0169-5347(92)90144-Z CrossRefGoogle Scholar
  88. Papke RT, Ward DM (2004) The importance of physical isolation to microbial diversification. FEMS Microbiol Ecol 48:293–303. doi:10.1016/j.femsec.2004.03.013 CrossRefPubMedGoogle Scholar
  89. Perez SF, Cook CB, Brooks WR (2001) The role of symbiotic dinoflagellates in the temperature induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256:1–14. doi:10.1016/S0022-0981(00)00282-3 PubMedCrossRefGoogle Scholar
  90. Pineda J (1994) Internal tidal bores in the nearshore: warm-water fronts, seaward gravity currents and the onshore transport of neustonic larvae. J Mar Res 52:427–458. doi:10.1357/0022240943077046 CrossRefGoogle Scholar
  91. Pitts PA (1994) An investigation of Near-bottom flow patterns along and across Hawk Channel, Florida Keys. Bull Mar Sci 54:610–620Google Scholar
  92. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30. doi:10.1016/j.ympev.2005.04.028 PubMedCrossRefGoogle Scholar
  93. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P, Tunlid A, Hagstrom A (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16:867–880. doi:10.1111/j.1365-294X.2006.03189.x PubMedCrossRefGoogle Scholar
  94. Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE 3:e2160. doi:10.1371/journal.pone.0002160 PubMedCrossRefGoogle Scholar
  95. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  96. Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454. doi:10.1126/science.278.5342.1454 PubMedCrossRefGoogle Scholar
  97. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x CrossRefGoogle Scholar
  98. Rousset F (1997) Genetic differentiation and estimation of gene flow from F statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  99. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x CrossRefGoogle Scholar
  100. Rowan R (2004) Thermal adaptations in reef coral symbionts. Nature 430:742. doi:10.1038/430742a PubMedCrossRefGoogle Scholar
  101. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853. doi:10.1073/pnas.92.7.2850 PubMedCrossRefGoogle Scholar
  102. Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73. doi:10.3354/meps071065 CrossRefGoogle Scholar
  103. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733. doi:10.1111/j.1365-294X.2007.03403.x PubMedCrossRefGoogle Scholar
  104. Sanchez JA, Zea S, Diaz JM (1998) Patterns of octocoral and black coral distribution in the oceanic barrier reef-complex of Providencia Island, Southwestern Caribbean. Caribb J Sci 34:250–264Google Scholar
  105. Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204:10–20. doi:10.2307/1543491 PubMedCrossRefGoogle Scholar
  106. Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111. doi:10.1016/S1055-7903(02)00010-6 PubMedCrossRefGoogle Scholar
  107. Santos SR, Gutierrez-Rodriguez C, Coffroth MA (2003a) Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23 s)-ribosomal DNA sequences. Mar Biotechnol 5:130–140PubMedGoogle Scholar
  108. Santos SR, Gutierrez-Rodriguez C, Lasker HR, Coffroth MA (2003b) Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Mar Biol (Berl) 143:111–120. doi:10.1007/s00227-003-1065-0 CrossRefGoogle Scholar
  109. 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. doi:10.1046/j.1365-294X.2003.02058.x PubMedCrossRefGoogle Scholar
  110. Schoenberg DA, Trench RK (1980a) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc Lond B Biol Sci 207:405–427. doi:10.1098/rspb.1980.0031 CrossRefGoogle Scholar
  111. Schoenberg DA, Trench RK (1980b) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. II. Morphological variation in Symbiodinium microadriaticum. Proc R Soc Lond B Biol Sci 207:429–444. doi:10.1098/rspb.1980.0032 CrossRefGoogle Scholar
  112. Schoenberg DA, Trench RK (1980c) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc R Soc Lond B Biol Sci 207:445–460. doi:10.1098/rspb.1980.0033 CrossRefGoogle Scholar
  113. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90. doi:10.1139/z91-013 CrossRefGoogle Scholar
  114. Seyfert AL, Cristescu MEA, Frisse L, Schaack S, Thomas WK, Lynch M (2008) The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex. Genetics 178:2113–2121. doi:10.1534/genetics.107.081927 PubMedCrossRefGoogle Scholar
  115. Shearer TL, Coffroth MA (2006) Genetic identification of Caribbean scleractinian coral recruits at the Flower Garden Banks and the Florida Keys. Mar Ecol Prog Ser 306:133–142. doi:10.3354/meps306133 CrossRefGoogle Scholar
  116. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  117. Smith NP (1994) Long-term Gulf-to-Atlantic transport through tidal currents in the Florida Keys. Bull Mar Sci 54:602–609Google Scholar
  118. Smith N (1998) Tidal and long-term exchanges through channels in the Middle and Upper Florida Keys. Bull Mar Sci 62:199–211Google Scholar
  119. Smith JE, Smith CM, Vroom PS, Beach KL, Miller S (2004) Nutrient and growth dynamics of Halimeda tuna on Conch Reef, Florida Keys: possible influence of internal tides on nutrient status and physiology. Limnol Oceanogr 49:1923–1936Google Scholar
  120. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 4:627–632. doi:10.2307/2413122 CrossRefGoogle Scholar
  121. Sponaugle S, Lee TN, Kourafalou V, Pinkard D (2005) Florida Current frontal eddies and the settlement of coral reef fishes. Limnol Oceanogr 50:1033–1048Google Scholar
  122. Stat M, Gates RD (2008) Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii. Biol Invasions 10:579–583. doi:10.1007/s10530-007-9167-0 CrossRefGoogle Scholar
  123. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, dinophyta). J Phycol 40:160–164Google Scholar
  124. Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42:285–291CrossRefGoogle Scholar
  125. Taylor DL (1974) Symbiotic marine algae: taxonomy and biological fitness. In: Vernberg WB (ed) Symbiosis in the Sea. University of South Carolina Press, Columbia, pp 245–262Google Scholar
  126. Taylor FJR (1987) The biology of dinoflagellates. Blackwell, OxfordGoogle Scholar
  127. 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. doi:10.2307/1543613 PubMedCrossRefGoogle Scholar
  128. Ulstrup KE, Berkelmans R, Ralph PJ, van Oppen MJH (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314:135–148. doi:10.3354/meps314135 CrossRefGoogle Scholar
  129. Ulstrup KE, Hill R, van Oppen MJH, Larkum AWD, Ralph PJ (2008) Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Mar Ecol Prog Ser 361:139–150. doi:10.3354/meps07360 CrossRefGoogle Scholar
  130. van Oppen MJH, Mieog JC, Sanchez CA, Fabricius KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417. doi:10.1111/j.1365-294X.2005.02545.x PubMedCrossRefGoogle Scholar
  131. Wainwright SA, Dillon JR (1969) On the orientation of sea fans (genus Gorgonia). Biol Bull 136:130–139. doi:10.2307/1539674 CrossRefGoogle Scholar
  132. Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897Google Scholar
  133. Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10:436–448. doi:10.1006/mpev.1998.0546 PubMedCrossRefGoogle Scholar
  134. Willemsen JF (2005) Ocean circulation and impacts on plankton near the Florida Keys. Physica A 357:36–43. doi:10.1016/j.physa.2005.05.069 CrossRefGoogle Scholar
  135. Yacobovitch T, Benayahu Y, Weis VM (2004) Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). J Exp Mar Biol Ecol 298:35–48. doi:10.1016/j.jembe.2003.08.003 CrossRefGoogle Scholar
  136. Yeung C, Lee TN (2002) Larval transport and retention of the spiny lobster, Panulirus argus, in the coastal zone of the Florida Keys, USA. Fish Oceanogr 11:286–309. doi:10.1046/j.1365-2419.2002.00209.x CrossRefGoogle Scholar
  137. Yeung C, Jones DJ, Criales MM, Jackson TL, Richards WJ (2001) Influence of coastal eddies and counter-currents on the influx of spiny lobster, Panuliris argus, postlarvae into Florida Bay. Mar Freshw Res 52:1217–1232. doi:10.1071/MF01110 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Nathan L. Kirk
    • 1
    • 3
  • Jason P. Andras
    • 2
  • C. Drew Harvell
    • 2
  • Scott R. Santos
    • 3
  • Mary Alice Coffroth
    • 4
  1. 1.Department of Biological Sciences, 109 Cooke HallUniversity at Buffalo (State University of New York)BuffaloUSA
  2. 2.Department of Ecology and Evolutionary Biology, Corson HallCornell UniversityIthacaUSA
  3. 3.Department of Biological Sciences, 101 Life SciencesAuburn UniversityAuburnUSA
  4. 4.Department of Geology, 411 Cooke HallUniversity at Buffalo (State University of New York)BuffaloUSA

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