Marine Biotechnology

, Volume 12, Issue 5, pp 594–604 | Cite as

Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching

  • Francois O. Seneca
  • Sylvain Forêt
  • Eldon E. Ball
  • Carolyn Smith-Keune
  • David J. Miller
  • Madeleine J. H. van Oppen
Original Article

Abstract

Coral bleaching is a major threat to coral reefs worldwide and is predicted to intensify with increasing global temperature. This study represents the first investigation of gene expression in an Indo-Pacific coral species undergoing natural bleaching which involved the loss of algal symbionts. Quantitative real-time polymerase chain reaction experiments were conducted to select and evaluate coral internal control genes (ICGs), and to investigate selected coral genes of interest (GOIs) for changes in gene expression in nine colonies of the scleractinian coral Acropora millepora undergoing bleaching at Magnetic Island, Great Barrier Reef, Australia. Among the six ICGs tested, glyceraldehyde 3-phosphate dehydrogenase and the ribosomal protein genes S7 and L9 exhibited the most constant expression levels between samples from healthy-looking colonies and samples from the same colonies when severely bleached a year later. These ICGs were therefore utilised for normalisation of expression data for seven selected GOIs. Of the seven GOIs, homologues of catalase, C-type lectin and chromoprotein genes were significantly up-regulated as a result of bleaching by factors of 1.81, 1.46 and 1.61 (linear mixed models analysis of variance, P < 0.05), respectively. We present these genes as potential coral bleaching response genes. In contrast, three genes, including one putative ICG, showed highly variable levels of expression between coral colonies. Potential variation in microhabitat, gene function unrelated to the stress response and individualised stress responses may influence such differences between colonies and need to be better understood when designing and interpreting future studies of gene expression in natural coral populations.

Keywords

Coral bleaching Molecular stress response Gene expression Quantitative PCR Internal control gene Inter-colony variability 

Supplementary material

10126_2009_9247_Fig4_ESM.jpg (428 kb)
Table S1

Primers used for the genes under investigation in the qPCR experiment. The best Tblastx match and E value are shown for the EST sequence corresponding to the indicated accession number. The Symbiodinium-specific PCNA primers were designed on the same sequences used in Boldt et al. (2009) (JPEG 428 kb)

10126_2009_9247_Fig1_ESM.eps (602 kb)
Table S1High resolution image (EPS 601 kb)
10126_2009_9247_Fig5_ESM.jpg (98 kb)
Table S2

Ranking of the candidate ICGs according to their M and CV values (Hellemans et al. 2007) calculated between healthy-looking and severely bleached samples across the nine colonies used in qPCR experiment (JPEG 97 kb)

10126_2009_9247_Fig2_ESM.eps (313 kb)
Table S2High resolution image (EPS 313 kb)
10126_2009_9247_MOESM3_ESM.pdf (1.6 mb)
Table S3The Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) checklist for reviewers and editors (Bustin et al. 2009) (PDF 1669 kb)
10126_2009_9247_Fig6_ESM.jpg (505 kb)
Figure S1

Consistent difference between average quantification cycles of healthy (dark grey) and bleached (light grey) samples in nine colonies, for the best performing ICGs: GAPDH, rpL9 and S7 (JPEG 505 kb)

10126_2009_9247_Fig4_ESM.eps (418 kb)
Figure S1High resolution image (EPS 418 kb)

References

  1. Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Matz MV (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE 3:e2680CrossRefPubMedGoogle Scholar
  2. Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (eds) (2008) Climate Change and Water. Technical Paper of the Intergovernmental Panel on Climate Change, IPCC Secretariat, Geneva: pp 210 Google Scholar
  3. Bay LK, Nielsen HB, Jarmer H, Seneca FO, van Oppen MJ (2009a) Transcriptomic variation in a coral reveals pathways of clonal organisation. Marine Genomics 2:119–125Google Scholar
  4. Bay LK, Ulstrup KE, Nielsen HB, Jarmer H, Goffard N, Willis BL, Miller DJ, van Oppen MJH (2009b) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora. Mol Ecol 18:3062–3075CrossRefPubMedGoogle Scholar
  5. Beltran-Ramirez V (2008) Molecular aspects of the coral–algal symbiosis. Thesis, James Cook University, Townsville, AustraliaGoogle Scholar
  6. Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219–228CrossRefGoogle Scholar
  7. Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83CrossRefGoogle Scholar
  8. Boldt L, Yellowlees D, Dove S, Leggat B (2009) The effect of fluctuating light on Symbiodinium photosynthetic gene expression. Abstracts of 11th International Coral Reef Symposium, Fort Lauderdale, Florida, USA. July 7–July 11, 2008, p 29Google Scholar
  9. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta (G) 1760:1690–1695Google Scholar
  10. Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363CrossRefPubMedGoogle Scholar
  11. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  12. Brown BE, Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122:655–663CrossRefGoogle Scholar
  13. Brown BE, Downs CA, Dunne RP, Gibb SW (2002) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar Ecol Prog Ser 242:119–129CrossRefGoogle Scholar
  14. Bustin S (2004) Quantification of nucleic acids by PCR. In: A–Z of quantitative PCR, Vol. International University Line, La Jolla, CA, USAGoogle Scholar
  15. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622CrossRefPubMedGoogle Scholar
  16. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  17. Császár NBM, Seneca FO, van Oppen MJ (2009) Variation in expression levels of antioxidant genes in the scleractinian coral Acropora millepora under laboratory thermal stress conditions. Mar Ecol Prog Ser 392:93–102Google Scholar
  18. Demidenko E (2004) Mixed models, theory and application, Wiley-Interscience, HobokenCrossRefGoogle Scholar
  19. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971CrossRefPubMedGoogle Scholar
  20. Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116CrossRefGoogle Scholar
  21. Dove S, Takabayashi M, Hoegh-Guldberg O (1995) Isolation and partial characterization of the pink and blue pigments of Pocilloporid and Acroporid corals. Biol Bull 189:288–297CrossRefGoogle Scholar
  22. Dove SG, Hoegh-Guldberg O, Ranganathan S (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19:197–204CrossRefGoogle Scholar
  23. Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51:1149–1158CrossRefGoogle Scholar
  24. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543CrossRefPubMedGoogle Scholar
  25. Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53CrossRefGoogle Scholar
  26. Dykens JA, Shick M (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580CrossRefGoogle Scholar
  27. Edge SE, Morgan MB, Gleason DF, Snell TW (2005) Development of a coral cDNA array to examine gene expression profiles in Montastraea faveolata exposed to environmental stress. Mar Pollut Bull 51:507–523CrossRefPubMedGoogle Scholar
  28. Edge SE, Morgan MB, Snell TW (2008) Temporal analysis of gene expression in a field population of the Scleractinian coral Montastraea faveolata. J Exp Mar Biol Ecol 355:114–124CrossRefGoogle Scholar
  29. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65CrossRefGoogle Scholar
  30. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130CrossRefGoogle Scholar
  31. Gilmore AM, Larkum AWD, Salih A, Itoh S, Shibata Y, Bena C, Yamasaki H, Papina M, van Woesik R (2003) Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem Photobiol 77:515–523CrossRefPubMedGoogle Scholar
  32. Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17CrossRefGoogle Scholar
  33. Grasso L, Maindonald J, Rudd S, Hayward D, Saint R, Miller D, Ball E (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics 9:540CrossRefPubMedGoogle Scholar
  34. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci U S A 103:14288–14293CrossRefPubMedGoogle Scholar
  35. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19CrossRefPubMedGoogle Scholar
  36. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  37. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci U S A 89:10302–10305CrossRefPubMedGoogle Scholar
  38. Jeffrey SW, Haxo FT (1968) Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol Bull 135:149–165CrossRefGoogle Scholar
  39. Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162CrossRefGoogle Scholar
  40. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  41. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Roy Soc Lond B Biol Sci 275:1359–1365CrossRefGoogle Scholar
  42. Kawaguti S (1944) On the physiology of reef corals. VI. Study on the pigments. Palao Tropical Biology Station 2:616–673Google Scholar
  43. Kiss-Toth E, Bagstaff SM, Sung HY, Jozsa V, Dempsey C, Caunt JC, Oxley KM, Wyllie DH, Polgar T, Harte M, O’Neill LAJ, Qwarnstrom EE, Dower SK (2004) Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. J Biol Chem 279:42703–42708CrossRefPubMedGoogle Scholar
  44. Kvennefors ECE, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32:1582–1592CrossRefPubMedGoogle Scholar
  45. Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283CrossRefGoogle Scholar
  46. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  47. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253CrossRefPubMedGoogle Scholar
  48. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377CrossRefGoogle Scholar
  49. Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232CrossRefGoogle Scholar
  50. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–470CrossRefPubMedGoogle Scholar
  51. Matta JL, Trench RK (1991) The enzymatic response of the symbiotic dinoflagellate Symbiodinium microadriaticum (Freudenthal) to growth in vitro under varied oxygen tensions. Symbiosis 11:31–45Google Scholar
  52. Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Physiol Mol Integr Physiol 147:1–10CrossRefGoogle Scholar
  53. Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Resour 9:462–470CrossRefGoogle Scholar
  54. Maynard J, Baird A, Pratchett M (2008) Revisiting the Cassandra syndrome; the changing climate of coral reef research. Coral Reefs 27:745–749CrossRefGoogle Scholar
  55. Mazel CH (1995) Spectral measurements of fluorescence emission in Caribbean cnidarians. Mar Ecol Prog Ser 120:185–191CrossRefGoogle Scholar
  56. Mazel CH, Lesser MP, Gorbunov MY, Barry TM, Farrell JH, Wyman KD, Falkowski PG (2003) Green-fluorescent proteins in Caribbean corals. Limnol Oceanogr 48:402–411CrossRefGoogle Scholar
  57. Merle P-L, Sabourault C, Richier S, Allemand D, Furla P (2007) Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic Biol Med 42:236–246CrossRefPubMedGoogle Scholar
  58. Meyer E, Aglyamova G, Wang S, Buchanan-Carter J, Abrego D, Colbourne J, Willis B, Matz M (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GS-Flx. BMC Genomics 10:219CrossRefPubMedGoogle Scholar
  59. Miyawaki A (2002) Green fluorescent protein-like proteins in reef anthozoa animals. Cell Struct Funct 27:343–347CrossRefPubMedGoogle Scholar
  60. Mladenka P, Simunek T, Hubl M, Hrdina R (2006) The role of reactive oxygen and nitrogen species in cellular iron metabolism. Free Radic Res 40:263–272CrossRefPubMedGoogle Scholar
  61. Morgan MB, Edge SE, Snell TW (2005) Profiling differential gene expression of corals along a transect of waters adjacent to the Bermuda municipal dump. Mar Pollut Bull 51:524–533CrossRefPubMedGoogle Scholar
  62. Moya A, Tambutté S, Béranger G, Gaume B, Scimeca J-C, Allemand D, Zoccola D (2008) Cloning and use of a coral 36B4 gene to study the differential expression of coral genes between light and dark conditions. Mar Biotechnol 10:653–663CrossRefPubMedGoogle Scholar
  63. Muller E, Rogers C, Spitzack A, van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195CrossRefGoogle Scholar
  64. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  65. Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgen, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:445–456CrossRefGoogle Scholar
  66. Podesta GP, Glynn PW (2001) The 1997–98 El Nino event in Panama and Galapagos: an update of thermal stress indices relative to coral bleaching. Bull Mar Sci 69:43–59Google Scholar
  67. R_Development_Core_Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  68. Rebrikov D, Trofimov D (2006) Real-time PCR: a review of approaches to data analysis. Appl Biochem Microbiol 42:455–463CrossRefGoogle Scholar
  69. Richier S, Merle P-L, Furla P, Pigozzi D, Sola F, Allemand D (2003) Characterization of superoxide dismutases in anoxia- and hyperoxia-tolerant symbiotic cnidarians. Biochim Biophys Acta (G) 1621:84–91Google Scholar
  70. Rodriguez-Lanetty M, Phillips WS, Dove S, Hoegh-Guldberg O, Weis VM (2008) Analytical approach for selecting normalizing genes from a cDNA microarray platform to be used in q-RT-PCR assays: a cnidarian case study. J Biochem Biophys Methods 70:985–991CrossRefPubMedGoogle Scholar
  71. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269CrossRefPubMedGoogle Scholar
  72. Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853CrossRefPubMedGoogle Scholar
  73. Schlichter D, Fricke HW (1990) Coral host improves photosynthesis of endosymbiotic algae. Naturwissenschaften 77:447–450CrossRefGoogle Scholar
  74. Shigeta M, Sanzen N, Ozawa M, Gu J, Hasegawa H, Sekiguchi K (2003) CD151 regulates epithelial cell–cell adhesion through PKC- and Cdc42-dependent actin cytoskeletal reorganization. J Cell Biol 163:165–176CrossRefPubMedGoogle Scholar
  75. Smith C (2005) The role of genetic and environmental variation on thermal tolerance of a reef-building coral, Acropora millepora. Thesis, University of Queensland, Brisbane, AustraliaGoogle Scholar
  76. Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10:166–180CrossRefPubMedGoogle Scholar
  77. Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol 11:1–11CrossRefGoogle Scholar
  78. Sunagawa S, Wilson E, Thaler M, Smith M, Caruso C, Pringle J, Weis V, Medina M, Schwarz J (2009) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10:258CrossRefPubMedGoogle Scholar
  79. Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, 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 U S A 101:13531–13535CrossRefPubMedGoogle Scholar
  80. Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639CrossRefPubMedGoogle Scholar
  81. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–11CrossRefGoogle Scholar
  82. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883CrossRefPubMedGoogle Scholar
  83. Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Ferrier-Pages C, Tambutte E, Tambutte S, Zoccola D, Allemand D, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiology 9:14CrossRefPubMedGoogle Scholar
  84. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, Szmant AM, Coffroth MA, Medina M (2009) The host transcriptome remains unaltered during the establishment of coral–algal symbioses. Mol Ecol 18:1823–1833CrossRefPubMedGoogle Scholar
  85. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012CrossRefPubMedGoogle Scholar
  86. Whanger PD (2000) Selenoprotein W: a review. Cell Mol Life Sci 57:1846–1852CrossRefPubMedGoogle Scholar
  87. Wiedenmann J, Ivanchenko S, Oswald F, Nienhaus GU (2004) Identification of GFP-like proteins in nonbioluminescent, azooxanthellate anthozoa opens new perspectives for bioprospecting. Mar Biotechnol 6:270–277CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Francois O. Seneca
    • 1
    • 2
    • 3
  • Sylvain Forêt
    • 5
  • Eldon E. Ball
    • 4
  • Carolyn Smith-Keune
    • 3
    • 6
    • 7
  • David J. Miller
    • 1
    • 2
  • Madeleine J. H. van Oppen
    • 3
  1. 1.Coral Genomics GroupJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.Australian Institute of Marine ScienceTownsville MCAustralia
  4. 4.ARC Centre for the Molecular Genetics of Development, Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  5. 5.Mathematical Science InstituteAustralian National UniversityCanberraAustralia
  6. 6.Aquaculture Genetics GroupJames Cook UniversityTownsvilleAustralia
  7. 7.Centre for Marine StudiesUniversity of QueenslandSt LuciaAustralia

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