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

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Abstract

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.

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References

  • Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand

    Google Scholar 

  • 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 23:4418–4433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol S 40:551–571

    Article  Google Scholar 

  • Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141

    Article  PubMed  Google Scholar 

  • 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 21:1897–1908

    Article  PubMed  Google Scholar 

  • Bowen BW, Rocha LA, Toonen RJ, Karl SA, Laboratory ToBo (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366

    Article  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603

    Article  Google Scholar 

  • 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: http://www.geneious.com

  • 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:e44970

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fenner D (2005) Corals of Hawaii. Mutual Publishing, Honolulu, HI

    Google Scholar 

  • 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 12:369–373

    Article  PubMed  Google Scholar 

  • 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 117:239–250

    Article  CAS  Google Scholar 

  • Huelsenbeck J, Ronquist F (2001) MRBAYES: a program for the Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Koeppel AF, Wu M (2013) Surprisingly extensive mixed phylogenetic and ecological signals among bacterial operational taxonomic units. Nucleic Acids Res 41:5175–5188

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 48:2046–2054

    Article  Google Scholar 

  • 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 23:596–603

    Google Scholar 

  • 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 53:305–319

    Article  Google Scholar 

  • 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 284:147–161

    Article  Google Scholar 

  • 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 37:785–800

    Article  Google Scholar 

  • Law R (1985) Evolution in a mutualistic environment. In: Boucher DH (ed) The biology of mutualism. Oxford University Press, Oxford, UK, pp 145–191

    Google Scholar 

  • 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 58:211–230

    Article  Google Scholar 

  • NOAA Coral Reef Watch (2000) Coral Reef Watch 50-km satellite time series data. Silver Spring, Maryland, USA. http://coralreefwatch.noaa.gov/satellite/sst.php

  • 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 434–435:71–80

    Article  Google Scholar 

  • Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898

    Article  CAS  PubMed  Google Scholar 

  • Parker MA (1999) Mutualism in metapopulations of legumes and Rhizobia. Am Nat 153:48–60

    Article  Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawaii. Mol Phylogenet Evol 56:492–497

    Article  CAS  PubMed  Google Scholar 

  • 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 139:1069–1078

    Article  Google Scholar 

  • 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 19:4661–4677

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • 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 83–108

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519

    Article  CAS  PubMed  Google Scholar 

  • 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 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Selkoe KA, Gaggiotti OE, Laboratory ToBo, Bowen BW, Toonen RJ (2014) Emergent patterns of population genetic structure for a coral reef community. Mol Ecol 23:3064–3079

    Article  PubMed  Google Scholar 

  • 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 27:763–772

    Article  Google Scholar 

  • Stat M, Pochon X, Cowie OM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston atoll. Mar Ecol Prog Ser 386:83–96

    Article  CAS  Google Scholar 

  • 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 3:1317–1329

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 63:1–65

    Article  PubMed  Google Scholar 

  • 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 157:31–43

    Article  CAS  PubMed  Google Scholar 

  • Swofford D (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, MA. Available at: http//paup.csit.fsu.edu/

  • 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 23:3133–3136

    Article  Google Scholar 

  • Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14

    Article  Google Scholar 

  • Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738

    Article  CAS  PubMed  Google Scholar 

  • Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367

    Article  CAS  PubMed  Google Scholar 

  • 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 2011:460173

    Article  PubMed Central  PubMed  Google Scholar 

  • Wagner WL, Funk VA (1995) Hawaiian biogeography: evolution on a hotspot archipelago. Smithsonian Institute Press, Washington, DC

    Google Scholar 

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Acknowledgments

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.

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Correspondence to Michael Stat.

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Communicated by Biology Editor Dr. Simon Davy

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Stat, M., Yost, D.M. & Gates, R.D. Geographic structure and host specificity shape the community composition of symbiotic dinoflagellates in corals from the Northwestern Hawaiian Islands. Coral Reefs 34, 1075–1086 (2015). https://doi.org/10.1007/s00338-015-1320-0

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