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Unique combinations of coral host and algal symbiont genotypes reflect intraspecific variation in heat stress responses among colonies of the reef-building coral, Montipora digitata

Abstract

High temperatures disrupt coral–algal symbioses in multiple ways, with negative impacts on the physiology of the coral host, the algal symbiont, and the combined holobiont. Most heat stress studies on hard corals have understandably focused on species trends based on the combined observation of multiple individuals to account for phenotypic plasticity among colonies. As the “average coral” continues to decline while sea temperatures rise, the outlier colonies that exhibit neutral or positive responses to heat stress are coming to represent larger proportions of marginal coral populations. These colonies are those most likely to guide the future trajectory of reef ecosystems, but their dynamics are often obscured by aggregate analyses. To directly measure and analyze intraspecific variation in heat stress responses within a natural coral population, we performed aquarium experiments on sixteen colonies of the structurally important branching coral Montipora digitata from Okinawa Island, Japan. We resolved host and symbiont genotypes, exposed replicate coral fragments to ambient or elevated temperature, and monitored stress-driven differences in host calcification, symbiont photochemistry, and colony mortality. Over the 6-month experiment, six colonies appeared to tolerate stress (exhibiting no major physiological changes), seven were sensitive to stress (exhibiting reduced growth), and three expired. Both host and symbiont genotype contributed to this variation. These results demonstrate the degree to which unique M. digitata holobionts may differentially respond to thermal stress in warming oceans and highlight the important role of intraspecific variation in shaping future reef assemblages.

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References

  1. Abrego D, Ulstrup 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

  2. Andersen PK, Gill RD (1982) Cox's regression model for counting processes: a large sample study. Ann Stat 10:1100–1120

  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689

  4. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

  5. 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

  6. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110:1387–1392

  7. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stats Softw 67:1–48

  8. Baums IB, Devlin-Durante MK, Polato NR, Xu D, Giri S, Altman NS, Ruiz D, Parkinson JE, Boulay JN (2013) Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata. Coral Reefs 32:703–717

  9. Baums IB, Baker AC, Davies SW, Grottoli AG, Kenkel CD, Kitchen SA, Kuffner IB, LaJeunesse TC, Matz MV, Miller MW, Parkinson JE, Shantz AA (2019) Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol Appl 29:e01978

  10. Bay RA, Palumbi SR (2015) Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol Evol 7:1602–1612

  11. Bayliss SL, Scott ZR, Coffroth MA, terHorst CP (2019) Genetic variation in Breviolum antillogorgium, a coral reef symbiont, in response to temperature and nutrients. Ecol Evol 9:2803–2813

  12. 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

  13. Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340

  14. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

  15. Brown BE, Dunne RP, Goodson MS, Douglas AE (2000) Marine ecology: bleaching patterns in reef corals. Nature 404:142–143

  16. Carballo-Bolaños R, Denis V, Huang Y-Y, Keshavmurthy S, Chen CA (2019) Temporal variation and photochemical efficiency of species in Symbiodiniaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS ONE 14:e0218801

  17. Concepcion GT, Polato NR, Baums IB, Toonen RJ (2010) Development of microsatellite markers from four Hawaiian corals: Acropora cytherea, Fungia scutaria, Montipora capitata and Porites lobata. Conserv Genet Resour 2:11–15

  18. Costa-Pereira R, Toscano B, Souza FL, Ingram T, Araújo MS (2019) Individual niche trajectories drive fitness variation. Funct Ecol 33:1734–1745

  19. Darling ES, McClanahan TR, Côté IM (2013) Life histories predict coral community disassembly under multiple stressors. Global Change Biol 19:1930–1940

  20. Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

  21. Denis V, Guillaume MM, Goutx M, de Palmas S, Debreuil J, Baker AC, Boonstra RK, Bruggemann JH (2013) Fast growth may impair regeneration capacity in the branching coral Acropora muricata. PLoS ONE 8:e72618

  22. Devlin-Durante M, Miller M, Precht W, Baums I (2016) How old are you? Genet age estimates in a clonal animal. Mol Ecol 25:5628–5646

  23. Devlin-Durante M, Baums I, Williams DW, Vohsen S, Kemp D (2019) What drives phenotypic divergence among coral clonemates of Acropora palmata? Mol Ecol 28:3208–3224

  24. Díaz-Almeyda EM, Prada C, Ohdera A, Moran H, Civitello D, Iglesias-Prieto R, Carlo T, LaJeunesse T, Medina M (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc R Soc B 284:20171767

  25. Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462

  26. Dziedzic K, Elder H, Tavalire HF, Meyer E (2019) Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata). Mol Ecol 28:2238–2253

  27. Edmunds PJ (2017) Intraspecific variation in growth rate is a poor predictor of fitness for reef corals. Ecology 98:2191–200

  28. Enrıquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032

  29. Forsman A, Wennersten L (2016) Inter-individual variation promotes ecological success of populations and species: evidence from experimental and comparative studies. Ecography 39:630–648

  30. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71

  31. Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:2280–2292

  32. Goreau TJ, Hayes RL (1994) Coral bleaching and ocean "hot spots". Ambio 23:176–180

  33. Goreau T, MacFarlane A (1990) Reduced growth rate of Montastraea annularis following the 1987–1988 coral-bleaching event. Coral Reefs 8:211–215

  34. Goreau T, McClanahan T, Hayes R, Strong A (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14:5–15

  35. Goreau T, Hayes R, Strong A (2005) Global coral reef bleaching and sea surface temperature trends from satellite-derived hotspot analysis. World Resour Rev 17:254–293

  36. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498

  37. Goulet TL, LaJeunesse TC, Fabricius KE (2008) Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar Biol 154:795–804

  38. Graham NA, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97

  39. Granados-Cifuentes C, Bellantuono AJ, Ridgway T, Hoegh-Guldberg O, Rodriguez-Lanetty M (2013) High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity. BMC Genom 14:228

  40. Gray B (2013) cmprsk: Subdistribution analysis of competing risks. R package

  41. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

  42. Grupstra CG, Coma R, Ribes M, Leydet KP, Parkinson JE, McDonald K, Catlla M, Voolstra CR, Hellberg ME, Coffroth MA (2017) Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 36:981–985

  43. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7:e33353

  44. Hawkins TD, Hagemeyer J, Warner ME (2016) Temperature moderates the infectiousness of two conspecific Symbiodinium strains isolated from the same host population. Environ Microbiol 18:5204–5217

  45. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, 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

  46. Hongo C, Yamano H (2013) Species-specific responses of corals to bleaching events on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15-year period (1995–2009). PLoS ONE 8:e60952

  47. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Change 2:116–120

  48. Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Global Change Biol 22:2702–2714

  49. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, Kleypas J, van de Leemput IA, Lough JM, Morrison TH (2017a) Coral reefs in the Anthropocene. Nature 546:82–90

  50. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017b) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

  51. Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Jacobson M, Liu G (2018) Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat Clim Change 9:40

  52. Hume BC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci USA 113:4416–4421

  53. Hunter C, Morden C, Smith C (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. In: Lessios HA, Macintyre IG (eds) Proceedings of the 8th international coral reef symposium, vol 2. Smithsonian Tropical Research Institute, Panama, pp 1599–1602

  54. Jokiel P, Coles S (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208

  55. Kavousi J, Reimer JD, Tanaka Y, Nakamura T (2015) Colony-specific investigations reveal highly variable responses among individual corals to ocean acidification and warming. Mar Environ Res 109:9–20

  56. Kavousi J, Parkinson JE, Nakamura T (2016a) Combined ocean acidification and low temperature stressors cause coral mortality. Coral Reefs 35:903–907

  57. Kavousi J, Tanaka Y, Nishida K, Suzuki A, Nojiri Y, Nakamura T (2016b) Colony-specific calcification and mortality under ocean acidification in the branching coral Montipora digitata. Mar Environ Res 119:161–165

  58. Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348

  59. Kubicek A, Breckling B, Hoegh-Guldberg O, Reuter H (2019) Climate change drives trait-shifts in coral reef communities. Sci Rep 9:3721

  60. Kuffner IB, Bartels E, Stathakopoulos A, Enochs IC, Kolodziej G, Toth LT, Manzello DP (2017) Plasticity in skeletal characteristics of nursery-raised staghorn coral, Acropora cervicornis. Coral Reefs 36:679–684

  61. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a "species" level marker. J Phycol 37:866–880

  62. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS ONE 6:e29013

  63. LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magana AL, Perez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc Lond B Biol 277:2925–2934

  64. LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391

  65. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

  66. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stats Softw 69:1–33

  67. Little AF, Van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

  68. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

  69. Matthews JL, Crowder CM, Oakley CA, Lutz A, Roessner U, Meyer E, Grossman AR, Weis VM, Davy SK (2017) Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proc Natl Acad Sci USA 114:13194–13199

  70. Matthews JL, Oakley CA, Lutz A, Hillyer KE, Roessner U, Grossman AR, Weis VM, Davy SK (2018) Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis. Proc R Soc B 285:20182336

  71. McClanahan T (2004) The relationship between bleaching and mortality of common corals. Mar Biol 144:1239–1245

  72. 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

  73. Morey RD, Rouder JN, Jamil T (2015) Package ‘BayesFactor’. R package version 0912–2

  74. Morikawa MK, Palumbi SR (2019) Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc Natl Acad Sci USA 116:10586–10591

  75. Nakamura T, Van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304

  76. Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Colony integration during regeneration in the stony coral Favia fragum. Ecology 82:802–813

  77. Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:445

  78. Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB (2015) Intraspecific diversity among partners drives functional variation in coral symbioses. Sci Rep 5:15667

  79. Parkinson JE, Bartels E, Devlin-Durante MK, Lustic C, Nedimyer K, Schopmeyer S, Lirman D, LaJeunesse TC, Baums IB (2018) Extensive transcriptional variation poses a challenge to thermal stress biomarker development for endangered corals. Mol Ecol 27:1103–1119

  80. Parkinson JE, Baker AC, Baums IB, Davies SW, Grottoli AG, Kitchen SA, Matz MV, Miller MW, Shantz AA, Kenkel CD (2019) Molecular tools for coral reef restoration: beyond biomarker discovery. Conserv Lett. https://doi.org/10.1111/conl.12687

  81. Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci USA 112:7513–7518

  82. Polato NR, Voolstra CR, Schnetzer J, DeSalvo MK, Randall CJ, Szmant AM, Medina M, Baums IB (2010) Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS ONE 5:e11221

  83. Polato NR, Altman NS, Baums IB (2013) Variation in the transcriptional response of threatened coral larvae to elevated temperatures. Mol Ecol 22:1366–1382

  84. Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372

  85. Putnam HM, Davidson JM, Gates RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol Appl 9:1165–1178

  86. Rouzé H, Lecellier G, Pochon X, Torda G, Berteaux-Lecellier V (2019) Unique quantitative Symbiodiniaceae signature of coral colonies revealed through spatio-temporal survey in Moorea. Sci Rep 9:7921

  87. Rowan R, Powers DA (1992) Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc Natl Acad Sci USA 89:3639–3643

  88. Sakai K (1998) Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol Bull 195:319–325

  89. 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

  90. Shaw EC, Carpenter RC, Lantz CA, Edmunds PJ (2016) Intraspecific variability in the response to ocean warming and acidification in the scleractinian coral Acropora pulchra. Mar Biol 163:210

  91. Stat M, Loh W, LaJeunesse T, Hoegh-Guldberg O, Carter D (2009) Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713

  92. Therneau T (2015) A package for survival analysis in S. version 2.38.

  93. Thornhill DJ, Fitt WK, Schmidt GW (2006a) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519

  94. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006b) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722

  95. Towle EK, Enochs IC, Langdon C (2015) Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE 10:e0123394

  96. Vago R, Dubinsky Z, Genin A, Ben-Zion M, Kizner Z (1997) Growth rates of three symbiotic corals in the Red Sea. Limnol Oceanogr 42:1814–1819

  97. Van Hooidonk R, Maynard J, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nat Clim Change 3:508–511

  98. Van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76

  99. Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252

  100. Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87–90

  101. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York

  102. Wright RM, Mera H, Kenkel CD, Nayfa M, Bay LK, Matz MV (2019) Positive genetic associations among fitness traits support evolvability of a reef-building coral under multiple stressors. Mol Ecol 25:3294–3304

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Acknowledgements

J.K. was supported by JGC-S Scholarship Foundation. J.E.P. was funded by a postdoctoral fellowship from the Japan Society for the Promotion of Science (JSPS). V.D. was supported by a grant from the Ministry of Science and Technology (Taiwan, no. 104–2611- M-002 -020 -MY2). T.N. was supported by JST/JICA, SATREPS. This work was sponsored in part by a JSPS ‘Zuno-Junkan’ grant entitled “Studies on origin and maintenance of marine biodiversity and systematic conservation planning” to J.D.R.

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Kavousi, J., Denis, V., Sharp, V. et al. Unique combinations of coral host and algal symbiont genotypes reflect intraspecific variation in heat stress responses among colonies of the reef-building coral, Montipora digitata. Mar Biol 167, 23 (2020). https://doi.org/10.1007/s00227-019-3632-z

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