Coral Reefs

, Volume 34, Issue 4, pp 1075–1086 | Cite as

Geographic structure and host specificity shape the community composition of symbiotic dinoflagellates in corals from the Northwestern Hawaiian Islands

  • Michael Stat
  • Denise M. Yost
  • Ruth D. Gates


How host–symbiont assemblages vary over space and time is fundamental to understanding the evolution and persistence of mutualistic symbioses. In this study, the diversity and geographic structure of coral–algal partnerships across the remote Northwestern Hawaiian Islands archipelago was investigated. The diversity of symbionts in the dinoflagellate genus Symbiodinium was characterised using the ribosomal internal transcribed spacer 2 (ITS2) gene in corals sampled at ten reef locations across the Northwestern Hawaiian Islands. Symbiodinium diversity was reported using operational taxonomic units and the distribution of Symbiodinium across the island archipelago investigated for evidence of geographic structure using permutational MANOVA. A 97 % sequence similarity of the ITS2 gene for characterising Symbiodinium diversity was supported by phylogenetic and ecological data. Four of the nine Symbiodinium evolutionary lineages (clades A, C, D, and G) were identified from 16 coral species at French Frigate Shoals, and host specificity was a dominant feature in the symbiotic assemblages at this location. Significant structure in the diversity of Symbiodinium was also found across the archipelago in the three coral species investigated. The latitudinal gradient and subsequent variation in abiotic conditions (particularly sea surface temperature dynamics) across the Northwestern Hawaiian Islands encompasses an environmental range that decouples the stability of host–symbiont assemblages across the archipelago. This suggests that local adaptation to prevailing environmental conditions by at least one partner in coral–algal mutualism occurs prior to the selection pressures associated with the maintenance of a symbiotic state.


Adaptation Biogeography Coral Hawaii ITS2 Symbiodinium 



This research was supported by the National Marine Sanctuary Program (memorandum of agreement 2005-008/66882), and a US National Science Foundation (NSF) Grant through Biological Oceanography (OCE-0752604). This is HIMB contribution # 1628 and SOEST contribution # 9438.

Supplementary material

338_2015_1320_MOESM1_ESM.xlsx (69 kb)
Supplementary material 1 (XLSX 68 kb)
338_2015_1320_MOESM2_ESM.docx (46 kb)
Supplementary material 2 (DOCX 46 kb)
338_2015_1320_MOESM3_ESM.docx (1.2 mb)
Supplementary material 3 (DOCX 1218 kb)
338_2015_1320_MOESM4_ESM.docx (109 kb)
Supplementary material 4 (DOCX 108 kb)
338_2015_1320_MOESM5_ESM.xlsx (78 kb)
Supplementary material 5 (XLSX 78 kb)


  1. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  2. Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barborrk A, Howe CJ, LaJeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433PubMedCentralCrossRefPubMedGoogle Scholar
  3. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol S 40:551–571CrossRefGoogle Scholar
  4. Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141CrossRefPubMedGoogle Scholar
  5. Blaalid R, Carlsen T, Kumar S, Halvorsen R, Ugland KI, Fontana G, Kauserud H (2012) Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21:1897–1908CrossRefPubMedGoogle Scholar
  6. Bowen BW, Rocha LA, Toonen RJ, Karl SA, Laboratory ToBo (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366CrossRefPubMedGoogle Scholar
  7. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  8. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603CrossRefGoogle Scholar
  9. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v6.1.6, Available at:
  10. Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD (2012) Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks. PLoS One 7:e44970PubMedCentralCrossRefPubMedGoogle Scholar
  11. Fenner D (2005) Corals of Hawaii. Mutual Publishing, Honolulu, HIGoogle Scholar
  12. Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol Ecol Resour 12:369–373CrossRefPubMedGoogle Scholar
  13. Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250CrossRefGoogle Scholar
  14. Huelsenbeck J, Ronquist F (2001) MRBAYES: a program for the Bayesian inference of phylogeny. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  15. Koeppel AF, Wu M (2013) Surprisingly extensive mixed phylogenetic and ecological signals among bacterial operational taxonomic units. Nucleic Acids Res 41:5175–5188PubMedCentralCrossRefPubMedGoogle Scholar
  16. LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene Transition. Mol Biol Evol 22:570–581CrossRefPubMedGoogle Scholar
  17. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054CrossRefGoogle Scholar
  18. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004a) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603Google Scholar
  19. LaJeunesse TC, Wham DC, Pettay DT, Parksinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) clade D are different species. Phycologia 53:305–319CrossRefGoogle Scholar
  20. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004b) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161CrossRefGoogle Scholar
  21. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (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 37:785–800CrossRefGoogle Scholar
  22. Law R (1985) Evolution in a mutualistic environment. In: Boucher DH (ed) The biology of mutualism. Oxford University Press, Oxford, UK, pp 145–191Google Scholar
  23. Maragos JE, Potts DC, Aeby GS, Gulko D, Kenyon JC, Siciliano D, van Ravenswaay D (2004) 2000-2002 rapid ecological assessments of corals (Anthozoa) on shallow reefs of the Northwestern Hawaiian Islands. Part 1: species and distribution. Pac Sci 58:211–230CrossRefGoogle Scholar
  24. NOAA Coral Reef Watch (2000) Coral Reef Watch 50-km satellite time series data. Silver Spring, Maryland, USA.
  25. Padilla-Gamino JL, Hanson KM, Stat M, Gates RD (2012) Phenotypic plasticity of the coral Porites rus: acclimatization responses to a turbid environment. J Exp Mar Bio Ecol 434–435:71–80CrossRefGoogle Scholar
  26. Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898CrossRefPubMedGoogle Scholar
  27. Parker MA (1999) Mutualism in metapopulations of legumes and Rhizobia. Am Nat 153:48–60CrossRefGoogle Scholar
  28. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawaii. Mol Phylogenet Evol 56:492–497CrossRefPubMedGoogle Scholar
  29. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  30. Polato NR, Concepcion GT, Toonen RJ, Baums IB (2010) Isolation by distance across the Hawaiian archipelago in the reef-building coral Porites lobata. Mol Ecol 19:4661–4677CrossRefPubMedGoogle Scholar
  31. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  32. Reaka-Kudla M (1997) The global biodiversity of coral reefs: A comparison with rainforests. In: Reaka-Kudla M, Wilson D, Wilson E (eds) Biodiversity II. Joseph Henry Press, Washington, DC, Understanding and protecting our biological resources, pp 83–108Google Scholar
  33. 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 138:1175–1181CrossRefGoogle Scholar
  34. Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519CrossRefPubMedGoogle Scholar
  35. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedCentralCrossRefPubMedGoogle Scholar
  36. Selkoe KA, Gaggiotti OE, Laboratory ToBo, Bowen BW, Toonen RJ (2014) Emergent patterns of population genetic structure for a coral reef community. Mol Ecol 23:3064–3079CrossRefPubMedGoogle Scholar
  37. Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA (2008) Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27:763–772CrossRefGoogle Scholar
  38. Stat M, Pochon X, Cowie OM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston atoll. Mar Ecol Prog Ser 386:83–96CrossRefGoogle Scholar
  39. Stat M, Pochon X, Franklin EC, Bruno JF, Casey KS, Selig ER, Gates RD (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3:1317–1329PubMedCentralCrossRefPubMedGoogle Scholar
  40. Stat M, Baker AC, Bourne DG, Correa AMS, Forsman Z, Huggett MJ, Pochon X, Skillings D, Toonen RJ, van Oppen MJH, Gates RD (2012) Molecular delineation of species in the coral holobiont. Adv Mar Biol 63:1–65CrossRefPubMedGoogle Scholar
  41. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31–43CrossRefPubMedGoogle Scholar
  42. Swofford D (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, MA. Available at: http// Scholar
  43. Thomas L, Kendrick GA, Kennington JW, Richards ZT, Stat M (2014) Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing. Mol Ecol 23:3133–3136CrossRefGoogle Scholar
  44. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14CrossRefGoogle Scholar
  45. Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738CrossRefPubMedGoogle Scholar
  46. Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367CrossRefPubMedGoogle Scholar
  47. Toonen RJ, Andrews KR, Baums IB, Bird CE, Concepcion GT, Daly-Engel TS, Eble JA, Faucci A, Gaither MR, Iacchei M, Puritz JB, Schultz JK, Skillings DJ, Timmers MA, Bowen BW (2011) Defining boundaries for ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian archipelago. J Mar Biol 2011:460173PubMedCentralCrossRefPubMedGoogle Scholar
  48. Wagner WL, Funk VA (1995) Hawaiian biogeography: evolution on a hotspot archipelago. Smithsonian Institute Press, Washington, DCGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Trace and Environmental DNA (TrEnD) Laboratory, Department of Environment and AgricultureCurtin UniversityPerthAustralia
  2. 2.Hawaii Institute of Marine Biology, School of Ocean and Earth Science and TechnologyUniversity of HawaiiKaneoheUSA

Personalised recommendations