Host genetics and symbiodinium D diversity in a stress-tolerant scleractinian coral, oulastrea crispata, in the west pacific

Marine Ecology Progress Series

Volumn 473, Issue , 2013, Pages 163-177

  Lien, Yi Ting ^a,g   Keshavmurthy, Shashank ^b   Nakano, Yoshikatsu ^c   Plathong, Sakanan ^d   Huang, Hui ^e   Hsu, Chia Mi ^b   Fukami, Hironobu ^f   Yamashita, Yoh ^g   Hsieh, Hernyi Justin ^h   Wang, Jih Tern ⁱ   Chen, Chaolun Allen ^b,j  

^a KYOTO UNIVERSITY   (Japan)

^b BIODIVERSITY RESEARCH CENTER   (Taiwan)

^c UNIVERSITY OF THE RYUKYUS   (Japan)

^d PRINCE OF SONGKLA UNIVERSITY   (Thailand)

^e SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^f UNIVERSITY OF MIYAZAKI   (Japan)

^g KYOTO UNIVERSITY   (Japan)

^h FISHERIES RESEARCH INSTITUTE   (Taiwan)

ⁱ TAJEN UNIVERSITY   (Taiwan)

^j ACADEMIA SINICA   (Taiwan)

more..

Author keywords

Clade D; Coral Symbiodinium; DGGE; Genetic subdivision; ITS; Stress tolerance

Indexed keywords

BIOGEOGRAPHICAL REGION; CLADISTICS; CORAL; ELECTROKINESIS; GENETIC STRUCTURE; GENETIC VARIATION; GEOGRAPHICAL DISTRIBUTION;

JAPAN; PACIFIC OCEAN; PACIFIC OCEAN (WEST); SOUTH CHINA SEA; THAILAND;

ANTHOZOA; OULASTREA CRISPATA; SCLERACTINIA; SYMBIODINIUM;

EID: 84872729975     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10041     Document Type: Article

References (64)

1. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34: 661-689 (Pubitemid 38171434)
2. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14: 1377-1390 (Pubitemid 40554795)
3. Baums IB, Johnson ME, Devlin-Durante MK, Miller MW (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida reef tract and wider Caribbean. Coral Reefs 29: 835-842
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 Biol Sci 273: 2305-2312 (Pubitemid 44387337)
5. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16: S129-S138
6. Chen CA (1999) Analysis of Scleractinian distribution in Taiwan indicating a pattern congruent with sea surface temperatures and currents: examples from Acropora and Faviidae corals. Zool Stud 38: 119-129 (Pubitemid 129328001)
7. Chen CA, Keshavmurthy S (2009) Taiwan as a connective stepping-stone in the Kuroshio Traiangle and the conservation of coral ecosystems under the impacts of climate change. Kuroshio Science 3: 15-22
8. Chen CA, Lam KK, Nakano Y, Tsai WS (2003) A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reef coral communities. Zool Stud 42: 540-550 (Pubitemid 37545854)
9. Chen CA, Ablan MCA, McManus JW, Bell JD, Tuan VS, Cabanban AS, Shao KT (2004) Population structure and genetic variability of six-bar wrasse (Thallasoma hard-wicki) in northern South China Sea revealed by mitochondrial control region sequences. Mar Biotechnol 6: 312-326 (Pubitemid 40047479)
10. Chen CA, Wang JT, Fang LS, Yang YW (2005a) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295: 113-121 (Pubitemid 41026816)
11. Chen CA, Yang YW, Wei NV, Tsai WS, Fang LS (2005b) Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24: 11-22
12. Dai CF, Fan TY, Yu JK (2000) Reproductive isolation and genetic differentiation of a scleractinian coral Mycedium elephantotus. Mar Ecol Prog Ser 201: 179-187
13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Applications to human mitochondrial DNA restriction data. Genetics 13: 479-491
14. Finney JC, Pettay DT, Sampayo EM, Warner WE, Oxenford HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60: 250-263
15. Goulet TL, Simmons C, Goulet D (2008) Worldwide bio geo -graphy of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355: 45-58 (Pubitemid 351449052)
16. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS and others (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742
17. IPCC (2007) Summary for policymakers. In: Solomon S, Qin D, Manning M (eds) Climate Change 2007: The physical science basis. Working group I contribution to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge, p 1-18
18. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community shift in the symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B Biol Sci 275: 1359-1365 (Pubitemid 351653015)
19. Keshavmurthy S, Hsu CM, Kuo CY, Meng PJ, Wang JT, Chen CA (2012) Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas.Mol Ecol 21: 4393-4407
20. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120 (Pubitemid 11166431)
21. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: The host as a habitat. Am Nat 162: S51-S62 (Pubitemid 37425177)
22. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400 (Pubitemid 36064320)
23. LaJeunesse TC (2005) Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J Phycol 41: 880-886 (Pubitemid 41197175)
24. LaJeunesse TC, Pinzón JH (2007) Screening intragenomic rDNA for dominant variants can provide a consistent retrieval of evolutionarily persistent ITS (rDNA) se -quences. Mol Phylogenet Evol 45: 417-422 (Pubitemid 47380422)
25. LaJeunesse TC, Trench RK (2000) Biogeography of 2 species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull (Woods Hole) 199: 126-134
26. LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc R Soc Lond B Biol Sci 276: 4139-4148
27. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N and others (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
28. Lam KK (2000) Sexual reproduction of a low-temperature tolerant coral Oulastrea crispata (Scleractinia, Faviidae) in Hong Kong, China. Mar Ecol Prog Ser 205: 101-111
29. Lien YT, Nakano Y, Plathong S, Fukami H, Wang JT, Chen CA (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26: 35-44 (Pubitemid 46491145)
30. Márquez LM, van Oppen MJH, Willis BL, Miller DJ (2002) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proc R Soc Lond B Biol Sci 269: 1289-1294 (Pubitemid 34734611)
31. Mackenzie JB, Munday PL, Willis BL, Miller DJ, van Oppen MJH (2004) Unexpected patterns of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Mol Ecol 13: 9-20 (Pubitemid 38106469)
32. Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14: 1861-1868 (Pubitemid 40772408)
33. Moothien Pillay KR, Asahida T, Chen CA, Terashima H, Ida H (2006) ITS ribosomal DNA distinctions and the genetic structures of populations of two sympatric species of Pavona (Cnidaria: Scleractinia) from Mauritius. Zool Stud 45: 132-144 (Pubitemid 43731770)
34. Myers R, Sheffield V, Cox D (1989) Mutation detection by PCR, GC-clamps, and denaturing gradient gel electrophoresis. In: Erlich HA (ed) PCR-technology -principles and applications for DNA amplification. Stockton Press, New York, NY, p 71-88
35. Nakajima Y, Nishikawa A, Isomura N, Iguchi A, Sakai K (2009) Genetic connectivity in the broadcast-spawning coral Acropora digitifera analyzed by microsatellite markers on the Sekisei Reef, southwestern Japan. Zool Sci 26: 209-215
36. Nakano Y, Yamazato K (1992) Ecological study of reproduction of Oulastrea crispata in Okinawa. Zool Sci 9: 1292
37. Nishikawa A, Sakai K (2003) Genetic variation and gene flow of broadcast spawning and planula brooding coral, Goniastrea aspera (Scleractinia) in the Ryukyu Archipelago, southern Japan. Zool Sci 20: 1031-1038 (Pubitemid 37195891)
38. Odorico D, Miller D (1997) Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol Biol Evol 14: 465-473 (Pubitemid 27200477)
39. Oliver TA, Palumbi SR (2011) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30: 241-250
40. 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 Resour 9: 1022-1025
41. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 56: 492-497
42. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225
43. Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) The phylogeography and connectivity of the latitudinally widespread scleractinian coral Plesiastrea versipora in the Western Pacific. Mol Ecol 11: 1177-1189 (Pubitemid 34793660)
44. 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 138: 1175-1181 (Pubitemid 32620738)
45. Rohlf FJ (1973) Algorithm 76. Hierarchical clustering using the minimum spanning tree. Comput J 16: 93-95
46. Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34: 407-417 (Pubitemid 28338345)
47. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430: 742 (Pubitemid 39071338)
48. Rozas J, Rozas R (1999) DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175 (Pubitemid 29134733)
49. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg 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
50. Schlötterer C, Hauser MT, von Haeseler A, Tautz D (1994) Comparative evolutionary analysis of rDNA ITS regions in Drosophila. Mol Biol Evol 11: 513-522 (Pubitemid 24137165)
51. SlatkinM(1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462
52. Smale DA, Wernberg T, Peck LS, Barnes KAD (2011) Turning on the heat: ecological response to simulated warming in the sea. PLoS ONE 6: e16050
53. Stat M, Gates RD (2011) Clade D Symbiodinium in scleractinian corals: A 'nugget' of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Biol 2011:730715
54. Takabayashi M, Carter DA, Lopez JV, Hoegh-Guldberg O (2003) Genetic variation of the scleractinian coral Stylophora pistillata, from western Pacific reefs. Coral Reefs 22: 17-22 (Pubitemid 36726138)
55. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882 (Pubitemid 28022245)
56. Thornhill DJ, LaJeunesse TC, Santos S (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16: 5326-5340 (Pubitemid 350265260)
57. 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 (Woods Hole) 201: 348-359 (Pubitemid 34057131)
58. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15: 3863-3883 (Pubitemid 44607139)
59. Veron JEN (1995) Corals in space and time: The biogeography and evolution of the Scleractinia. Cornell University Press, Ithaca, NY
60. Veron JEN, Stafford-Smith M (ed) (2000) Corals of the world. Australian Institute of Marine Science, Townsville
61. Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol Ecol 13: 2763-2772 (Pubitemid 39151632)
62. Wei NWV, Wallace CC, Dai CF, Moothien Pillay KR, Chen CA (2006) Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian Coral genus Acropora (Scleractinia; Acroporidae). Zool Stud 45: 404-418 (Pubitemid 44554061)
63. Wham DC, Pettay DT, LaJeunesse TC (2011) Microsatellite loci for the host-generalist 'zooxanthella' Symbiodinium trenchi and other clade D Symbiodinium. Conservation Genet Resour 3: 541-544
64. Yajima T, Sano O, Okamoto T, Yoshohiro S, Thutomu S, Masahiro M (1986) Ecological distribution of the reef coral, Oulastrea crispata (Lamarck) at the shore region in the vicinity of Tukumo Bay. Bull Jpn Sea Res Inst Kanazawa Univ 18: 21-36 (in Japanese)