Abstract
The evolutionary success and continued survival of reef-building corals under increasing environmental change will, in part, be determined by the composition of their endosymbiotic dinoflagellate communities (Symbiodinium sp.). Recent research suggests that differences in the phylotype composition of Symbiodinium in the same host can lead to different outcomes for the host when exposed to similar environmental conditions. One explanation for these observations is that symbioses between corals and Symbiodinium represent a continuum of interaction states that encompass mutualisms and parasitisms consistent with current evolutionary theory developed for other symbiotic systems. Here, we discuss the evidence supporting the existence of a parasitic to mutualistic continuum in Symbiodinium interactions and propose that a consideration of the evolutionary ecology of these associations will advance our understanding of how environmental change will influence the ecological outcomes in these important symbioses. We advocate that a robust taxonomic structure for Symbiodinium sp. and empirical studies on sexual reproduction in Symbiodinium, the stability of interaction states among Symbiodinium symbioses spatially and temporally and how interaction states change as the environment changes will generate data for models that accurately forecast how climate change will influence the persistence of corals and the reefs they structure.
References
Abrego D, Ulstruo KE, Willis BL, van Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond B 275:2273–2282
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689
Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity. Mol Ecol 19:1705–1720
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 273:2305–2312
Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science 229:656–658
Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ (2011) Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr 56:927–938
Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230
Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217
Brucker RM, Bordenstein SR (2012) Speciation by symbiosis. Trends Ecol Evol 27:443–451
Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high performance algal symbionts. Coral Reefs 28:405–414
Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261
de Bary A (1879) Die Erscheinung der Symbiose. Verlag von Karl J. Trubner, Strassburg
Donner SD (2009) Coping with commitment: projected thermal stress on coral reefs under different future scenarios. PLoS ONE 4:e5712
Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Global Change Biol 11:2251–2265
Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci USA 104:5483–5488
Douglas AE (2010) The symbiotic habit. Princeton University Press, Princeton p202
Douglas AE, Smith DC (1983) The cost of symbionts to their host in green Hydra. In: Schenk HEA, Schwemmler W (eds) Endocytobiology II Intracellular space as oligogenetic ecosystem. deGruyter, Berlin, pp 631–648
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
Fay SA, Weber MX (2012) The occurrence of mixed infections of Symbiodinium (Dinoflagellata) within individual hosts. J Phycol 48:1306–1316
Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110
Frank SA (1996) Models of parasitic virulence. Q Rev Biol 71:37–78
Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycles and morphology. Protozoology 9:45–52
Goff LJ (1982) Symbiosis and parasitism: another viewpoint. Bioscience 32:255–256
Golubski AJ, Klausmeier CA (2010) Control in mutualisms: combined implications of partner choice and bargaining roles. J Theor Biol 267:535–545
Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534
Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195
Hennige SJ, McGinley MP, Grottoli AG, Warner ME (2011) Photoinhibition of Symbiodinium spp. within the reef corals Montastraea faveolata and Porites astreoides: implications for coral bleaching. Mar Biol 158:2515–2526
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53
Hill M, Hill A (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biol Rev 87:804–821
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PJ, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2011) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim Change 2:116–120
Johnstone RA, Bshary R (2002) From parasitism to mutualism: partner control in asymmetric interactions. Ecol Lett 5:634–639
Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5:e10437
Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. J Mar Biol. doi:10.1155/2011/185890
Jones AM, Berkelmans R, van Oppen MJH, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B 275:1359–1365
Kinzie RA III, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumption. Biol Bull 200:51–58
LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
Lajeunesse TC (2004) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581
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 276:4139–4148
Leander BS, Keeling PJ (2004) Evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from HSP90 and actin phylogenies. J Phycol 40:341–350
Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–234
Leung TLF, Poulin R (2008) Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie Milieu-Life Environ 58:107–115
Lewin RA (1982) Symbiosis and parasitism-definitions and evaluations. Bioscience 32(254):256–260
Lewis DH (1985) Symbiosis and mutualism: crisp concepts and soggy semantics. In: Boucher DH (ed) Biology of mutualisms. Oxford University Press, New York, pp 29–39
Loram JE, Trapido-Rosenthal HG, Douglas AE (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol Ecol 16:4849–4857
Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364
Moran NA (2006) Symbiosis. Curr Biol 16:R866–R871
Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633
Moran NA, Werneberg JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15:321–326
Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from sortid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497
Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic genus Symbiodinium. Mol Phylogenet Evol 38:20–30
Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc Lond B 279:4352–4361
Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57–70
Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105:13674–13678
Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579
Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853
Rowan R, Powers DA (1991a) A molecular genetic classification of zooxanthellae and the evolution of the animal-algal symbioses. Science 251:1348–1351
Rowan R, Powers DA (1991b) Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc Natl Acad Sci USA 89:3639–3643
Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592
Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc Lond B 273:425–429
Sachs JL, Essenberg CJ, Turcotte MM (2011a) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202–209
Sachs JL, Skophammer RG, Regus JU (2011b) Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci USA 108:10800–10806
Savage AM, Trapido-Rosenthal HG, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244:27–37
Schwarz JA (2008) Understanding the intracellular niche in cnidarian-Symbiodinium symbioses: parasites lead the way. Vie Milieu-Life Environ 58:141–151
Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc R Soc Lond B 279:2609–2618
Star MP (1975) A generalized scheme for classifying organismic associations. Symp Soc Exp Biol 29:1–20
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. doi:10.1155/2011/730715
Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts - symbiosis, diversity, and the effect of climate change. Perspec Plant Ecol Evol Syst 8:23–43
Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105:9256–9261
Stat M, Baker AC, Bourne DG, Correa AMS, Forsman Z, Huggett M, Pochon X, Skillings D, Toonen R, van Oppen MJH, Gates RD (2012) Molecular delineation of species in the coral holobiont. Adv Mar Biol 63:1–65
Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker N (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956
Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164
Tchernov D, Gorbunov MY, de Vargas C, Yadav SW, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535
Toft C, Andersson SGE (2010) Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11:465–475
Trench RK, Blank RJ (1987) Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawaguti sp. nov., and S. pilosum sp. nov.: gymnodinoid dinoflagellate symbionts of marine invertebrates. J Phycol 23:469–481
van Oppen MJH (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar Biol 144:1–7
van Oppen MJH, Souter P, Howells EJ, Heyward A, Berkelmans R (2011) Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals. Diversity 3:405–423
van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76
Wisecaver JH, Hackett JM (2011) Dinoflagellate genome evolution. Annu Rev Microbiol 65:369–387
Wooldridge SA (2010) Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? BioEssays 32:615–625
Acknowledgments
The authors wish to thank many colleagues in the coral reef community, coming from many viewpoints, for their energetic discussions over the years that have stimulated critical thinking on the subject of this perspective. We also wish to thank the numerous funding sources that have continued to support our work on the biology and ecology of corals and coral reefs (NSF OCE-0752604 to RDG) and a postdoctoral fellowship to MS from the UWA-AIMS-CSIRO collaborative agreement. This is HIMB contribution number 1556 and SOEST contribution number 8952.
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Lesser, M.P., Stat, M. & Gates, R.D. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32, 603–611 (2013). https://doi.org/10.1007/s00338-013-1051-z
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DOI: https://doi.org/10.1007/s00338-013-1051-z