Genetic divergence across habitats in the widespread coral Seriatopora hystrixand its associated Symbiodinium

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Bongaerts, Pim ^a   Riginos, Cynthia ^a   Ridgway, Tyrone ^a,b   Sampayo, Eugenia M ^a,c   van Oppen, Madeleine J H ^d,e   Englebert, Norbert ^a   Vermeulen, Francisca ^a,f   Hoegh Guldberg, Ove ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GREAT BARRIER REEF MARINE PARK AUTHORITY   (Australia)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^e JAMES COOK UNIVERSITY   (Australia)

^f VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; RIBOSOME DNA;

ARTICLE; CONTROLLED STUDY; CORAL; CORAL REEF; DINOFLAGELLATE; DNA FRAGMENTATION; ENDOSYMBIOSIS; GENE LINKAGE DISEQUILIBRIUM; GENE STRUCTURE; GENETIC DIFFERENCE; GENETIC ISOLATION BY DISTANCE; GENETIC SIMILARITY; GENETIC VARIABILITY; HABITAT QUALITY; HABITAT STRUCTURE; HAPLOTYPE; MARINE SPECIES; MICROSATELLITE MARKER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REGULATOR GENE; SEQUENCE ALIGNMENT; SERIATOPORA HYSTRIX; SPECIES HABITAT; SYMBIODINIUM; SYMBIONT; UNINDEXED SEQUENCE;

ALGAE; ANTHOZOA; SERIATOPORA; SERIATOPORA HYSTRIX; SYMBIODINIUM;

EID: 77956518397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010871     Document Type: Article

References (89)

1. Mayr E (1954) Geographical Speciation In Tropical Echinoids. Evolution 8: 1-18.
2. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8: 336-352.
3. Johannesson K (2003) Evolution in Littorina: ecology matters. J Sea Res 49: 107-117.
4. Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14: 611-619.
5. Conde-Padín P, Carvajal-Rodriguez A, Carballo M, Caballero A, Rolán-Alvarez E (2007) Genetic variation for shell traits in a direct-developing marine snail involved in a putative sympatric ecological speciation process. Evol Ecol 21: 635-650.
6. Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in 40 years? Evolution. pp 1637-1653.
7. Ogden R, Thorpe RS (2002) Molecular evidence for ecological speciation in tropical habitats. Proc Natl Acad Sci USA 99: 13612-13615.
8. Richmond JQ, Reeder TW (2002) Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae). Evolution 56: 1498-1513.
9. Rundle HD, Schluter D (2004) Natural selection and ecological speciation in sticklebacks. In: Dieckmann U, Doebeli M, Metz JAJ, Tautz D, eds. Adaptive speciation. Cambridge: Cambridge University Press. pp 192-209.
10. Tonnis B, Grant PR, Grant BR, Petren K (2005) Habitat selection and ecological speciation in Galapagos warbler finches (Certhidea olivacea and Certhidea fusca). Proc R Soc, B 272: 819-826.
11. Langerhans RB, Gifford ME, Joseph EO (2007) Ecological speciation in Gambusia fishes. Evolution 61: 2056-2074.
12. Ryan PG, Bloomer P, Moloney CL, Grant TJ, Delport W (2007) Ecological speciation in South Atlantic island finches. Science 315: 1420-1423.
13. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc, B 272: 573-579.
14. Duran S, Rützler K (2006) Ecological speciation in a Caribbean marine sponge. Mol Phylogenet Evol 40: 292-297.
15. Rützler K, Duran S, Piantoni C (2007) Adaptation of reef and mangrove sponges to stress: evidence for ecological speciation exemplified by Chondrilla caribensis new species (Demospongiae, Chondrosida). Mar Ecol 28: 95-111.
16. Carlon DB, Budd AF, Bonhomme F (2002) Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56: 2227-2242.
17. Vermeij MJA, Bak RPM (2002) How are coral populations structured by light? Marine light regimes and the distribution of Madracis. Mar Ecol Prog Ser 233: 105-116.
18. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2: 495-509.
19. Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1: 95-107.
20. Monismith SG (2007) Hydrodynamics of coral reefs. Annual Rev Fluid Mech 39: 37-55.
21. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13: 15-155.
22. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83: 315-337.
23. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the 'deep reef refugia' hypothesis: focus on Caribbean reefs. Coral Reefs 29 (2): 309-327.
24. Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Syst 24: 189-216.
25. Knowlton N, Jackson JBC (1994) New taxonomy and niche partitioning on coral reefs: Jack of all trades or master of some? Trends Ecol Evol 1: 7-9.
26. Veron JEN, Stafford-Smith M (2000) Corals of the World: Australian Institute of Marine Science Townsville MC, Qld, Australia.
27. Diekmann OE, Bak RPM, Stam WT, Olsen JL (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar Biol 139: 221-233.
28. Vermeij MJA, Bak RPM (2003) Species-specific population structure of closely related coral morphospecies along a depth gradient (5-60 m) over a Caribbean reef slope. Bull Mar Sci 73: 725-744.
29. Bak RPM (1977) Coral reefs and their zonation in Netherlands Antilles. AAPG Studies in Geology 4: 3-16.
30. Van Moorsel G (1983) Reproductive strategies in two closely related stony corals (Agaricia, Scleractinia). Mar Ecol Prog Ser 13: 273-283.
31. Knowlton N, Weil E, Weigt LA, Guzman HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255: 330-333.
32. Lopez JV, Kersanach R, Rehner SA, Knowlton N (1999) Molecular determination of species boundaries in corals: genetic analysis of the Montastraea annularis complex using amplified fragment length polymorphisms and a microsatellite marker. Biol Bull 196: 80-93.
33. Ayre DJ, Veron JEN, Dufy SL (1991) The corals Acropora palifera and Acropora cuneata are genetically and ecologically distinct. Coral Reefs 10: 13-18.
34. Benzie JAH, Haskell A, Lehman H (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora palifera) populations from different reef habitats. Mar Biol 121: 731-739.
35. Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17: 2796-2811.
36. Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evolution. pp 1213-1228.
37. Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76: 503-519.
38. D'Croz L, Maté JL (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23: 473-483.
39. Vollmer SV, Kline DI (2008) Natural disease resistance in threatened staghorn corals. PLoS ONE 3: e3718.
40. Flot JF, Licuanan WY, Nakano Y, Payri C, Cruaud C, et al. (2008) Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs 27: 789-794.
41. Chen C, Dai CF, Plathong S, Chiou CY, Chen CA (2007) The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinia: Pocillo-poridae): an idiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations. Mol Phylogenet Evol 46: 19-33.
42. Flot JF, Magalon H, Cruaud C, Couloux A, Tillier S (2008) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes rendus-Biologies 331: 239-247.
43. Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ (2009) Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9: 45.
44. Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16: 771-784.
45. van Oppen MJH, Lutz A, De'ath G, Peplow L, Kininmonth S (2008) Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral. PLoS ONE 3: e3401.
46. Ayre DJ, Dufty S (1994) Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia's Great Barrier Reef. Evolution 48: 1183-1201.
47. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92: 2850-2853.
48. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16: 3721-3733.
49. Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17: 691-703.
50. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium. Annu Rev Ecol Syst 34: 661-689.
51. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, et al. (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23: 596-603.
52. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81: 599-603.
53. 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.
54. Stat M, Hoegh-Guldberg O, Fitt WK, Carter D (2008) Host symbiont acquisition strategy drives Symbiodinium diversity in the southern Great Barrier Reef. Coral Reefs 27: 763-772.
55. Veron JEN, Pichon M (1976) Scleractinia of eastern Australia, Part 1. Families Thamnasteriidae, Astrocoeniidae, and Pocilloporidae. Mar Sci Monogr Ser 1.
56. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution. pp 1590-1605.
57. Maier E, Tollrian R, Nürnberger B (2009) Fine-scale analysis of genetic structure in the brooding coral Seriatopora hystrix from the Red Sea. Coral Reefs 28: 751-756.
58. Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Evolution 54: 1590-1605.
59. Maier E, Tollrian R, Rinkevich B, Nürnberger B (2005) Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Mar Biol 147: 1109-1120.
60. Sherman CDH (2008) Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix. Heredity 100: 296-303.
61. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
62. LaJeunesse T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
63. Huston MA (1985) Patterns of species diversity on coral reefs. Annu Rev Ecol Syst 16: 149-177.
64. 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: 1887-1897.
65. 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: 23-27.
66. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc, B 271: 1757-1763.
67. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008) In situ photobiology of corals over large depth ranges: A multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53: 2711-2723.
68. Sampayo EM (2007) Diversity and ecology of Symbiodinium in pocilloporid corals. PhD thesis, The University of Queensland.
69. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts - symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8: 23-43.
70. Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proc 8th Int Coral Reef Symp 2: 1599-1602.
71. van Oppen MJ, Palstra FP, Piquet AM, Miller DJ (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 268: 1759-1767.
72. Diekmann O, Olsen J, Stam W, Bak R (2003) Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22: 29-33.
73. Loh WK, 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.
74. Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc, B 253: 167-171.
75. Schluter D (2000) The Ecology of Adaptive Radiation. Oxford: Oxford University Press.
76. Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates, Inc.
77. Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439: 719-723.
78. Savolainen V, Anstett MC, Lexer C, Hutton I Clarkson, et al. (2006) Sympatric speciation in palms on an oceanic island. Nature 441: 210-213.
79. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81: 2250-2263.
80. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.
81. Felsenstein, J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368-376.
82. Swofford DL (1999) PAUP 4.0: phylogenetic analysis using parsimony (and other methods). SunderlandMass: Sinauer.
83. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
84. Peakall R, Smouse PE (2001) GenAlEx V5: Genetic Analysis in Excel. Population Genetic Software for Teaching and Research, Australian National University.
85. Underwood JN, Souter PB, Ballment ER, Lutz AH, Van Oppen MJH (2006) Development of 10 polymorphic microsatellite markers from herbicide-bleached tissues of the brooding pocilloporid coral Seriatopora hystrix. Mol Ecol Notes 6: 176-178.
86. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18: 233-234.
87. 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.
88. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
89. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18: 117-143.