Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Rapid adaptive responses to climate change in corals

Abstract

Pivotal to projecting the fate of coral reefs is the capacity of reef-building corals to acclimatize and adapt to climate change. Transgenerational plasticity may enable some marine organisms to acclimatize over several generations and it has been hypothesized that epigenetic processes and microbial associations might facilitate adaptive responses. However, current evidence is equivocal and understanding of the underlying processes is limited. Here, we discuss prospects for observing transgenerational plasticity in corals and the mechanisms that could enable adaptive plasticity in the coral holobiont, including the potential role of epigenetics and coral-associated microbes. Well-designed and strictly controlled experiments are needed to distinguish transgenerational plasticity from other forms of plasticity, and to elucidate the underlying mechanisms and their relative importance compared with genetic adaptation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Identifying TGP in offspring depending on generational overlap in exposure.
Figure 2: Potential pathways that may enable TGP in corals include somatic, genetic and epigenetic factors of the coral gametes as well as their associated microbes transmitted vertically from one generation to the next.
Figure 3: Illustration showing members of the coral holobiont and their potential for contribution to adaptive holobiont responses.

Similar content being viewed by others

References

  1. IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2015).

  2. Bell, G. Evolutionary rescue and the limits of adaptation. Philos. Trans. R. Soc. B 368, 20120080 (2013).

    Google Scholar 

  3. Barrick, J. E. & Lenski, R. E. Genome dynamics during experimental evolution. Nat. Rev. Genet. 14, 827–839 (2013).

    CAS  Google Scholar 

  4. Munday, P. L., Warner, R. R., Monro, K., Pandolfi, J. M. & Marshall, D. J. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16, 1488–1500 (2013).

    Google Scholar 

  5. Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422 (2011).

    CAS  Google Scholar 

  6. Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    CAS  Google Scholar 

  7. Albright, R. et al. Reversal of ocean acidification enhances net coral reef calcification. Nature 531, 362–365 (2016).

    CAS  Google Scholar 

  8. Fabricius, K. E. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull. 50, 125–146 (2005).

    CAS  Google Scholar 

  9. Graham, N. A. J. & Nash, K. L. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326 (2013).

    Google Scholar 

  10. Fabricius, K. E., De'ath, G., Noonan, S. & Uthicke, S. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. B 281, 20132479 (2014).

    CAS  Google Scholar 

  11. Donelson, J. M., Munday, P. L., McCormick, M. I. & Pitcher, C. R. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2, 30–32 (2012). Seminal study demonstrating adaptive transgenerational plasticity to climate change in a coral-reef fish.

    Google Scholar 

  12. Putnam, H. M. & Gates, R. D. 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 (2015).

    Google Scholar 

  13. Daxinger, L. & Whitelaw, E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 20, 1623–1628 (2010). Critical review of evidence for transgenerational epigenetic inheritance.

    CAS  Google Scholar 

  14. Putnam, H. M., Davidson, J. M. & Gates, R. D. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9, 1165–1178 (2016). The only study to date that links environmental variation to epigenetic changes in corals.

    CAS  Google Scholar 

  15. Ptashne, M. Epigenetics: core misconcept. Proc. Natl Acad. Sci. USA 110, 7101–7103 (2013).

    CAS  Google Scholar 

  16. Boulotte, N. M. et al. Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J. 10, 2693–2701 (2016).

    CAS  Google Scholar 

  17. Webster, N. S. & Reusch, T. B. H. Microbial contributions to the persistence of coral reefs. ISME J. http://dx.doi.org/10.1038/ismej.2017.66 (2017).

  18. van Oppen, M. J. H., Souter, P., Howells, E. J., Heyward, A. & Berkelmans, R. Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals? Diversity 3, 405–423 (2011).

    CAS  Google Scholar 

  19. Agrawal, A. A., Laforsch, C. & Tollrian, R. Transgenerational induction of defences in animals and plants. Nature 401, 60–63 (1999).

    CAS  Google Scholar 

  20. Herman, J. J. & Sultan, S. E. Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front. Plant Sci. 2, 1–10 (2011).

    Google Scholar 

  21. Salinas, S., Brown, S. C., Mangel, M. & Munch, S. B. Non-genetic inheritance and changing environments. Non-Genet. Inherit. https://doi.org/10.2478/ngi-2013-0005 (2013).

  22. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014). Demonstrates the link between environmental change and gene expression levels, as well as rapid acclimatization in corals.

    CAS  Google Scholar 

  23. Moya, A. et al. Rapid acclimation of juvenile corals to CO2-mediated acidification by upregulation of heat shock protein and Bcl-2 genes. Mol. Ecol. 24, 438–452 (2015).

    CAS  Google Scholar 

  24. Veilleux, H. D. et al. Molecular processes of transgenerational acclimation to a warming ocean. Nat. Clim. Change 5, 1074–1078 (2015).

    CAS  Google Scholar 

  25. Goncalves, P. et al. Rapid transcriptional acclimation following transgenerational exposure of oysters to ocean acidification. Mol. Ecol. 25, 4836–4849 (2016).

    CAS  Google Scholar 

  26. Waddington, C. H. Organisers and Genes (Cambridge Univ. Press, 1940).

    Google Scholar 

  27. Wolff, G. L., Kodell, R. L., Moore, S. R. & Cooney, C. A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 12, 949–957 (1998).

    CAS  Google Scholar 

  28. Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K. & Whitelaw, E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314–318 (1999).

    CAS  Google Scholar 

  29. Metzger, D. C. H. & Schulte, P. M. Epigenomics in marine fishes. Mar. Genomics 30, 43–54 (2016).

    Google Scholar 

  30. Rakyan, V. K. et al. Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission. Proc. Natl Acad. Sci. USA 100, 2538–2543 (2003).

    CAS  Google Scholar 

  31. Klosin, A., Casas, E., Hidalgo-Carcedo, C., Vavouri, T. & Lehner, B. Transgenerational transmission of environmental information in C. elegans. Science 356, 320–323 (2017).

    CAS  Google Scholar 

  32. Libbrecht, R., Oxley, P. R., Keller, L. & Kronauer, D. J. C. Robust DNA methylation in the clonal raider ant brain. Curr. Biol. 26, 391–395 (2016).

    CAS  Google Scholar 

  33. Meng, D. et al. Limited contribution of DNA methylation variation to expression regulation in Arabidopsis thaliana. PLOS Genet. 12, e1006141 (2016).

    Google Scholar 

  34. Lyko, F., Ramsahoye, B. H. & Jaenisch, R. Development: DNA methylation in Drosophila melanogaster. Nature 408, 538–540 (2000).

    CAS  Google Scholar 

  35. Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465–476 (2008).

    CAS  Google Scholar 

  36. Bestor, T. H., Edwards, J. R. & Boulard, M. Notes on the role of dynamic DNA methylation in mammalian development. Proc. Natl Acad. Sci. USA 112, 6796–6799 (2015).

    CAS  Google Scholar 

  37. Dimond, J. L. & Roberts, S. B. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Mol. Ecol. 25, 1895–1904 (2016).

    CAS  Google Scholar 

  38. Dixon, G. B., Bay, L. K. & Matz, M. V. Evolutionary consequences of DNA methylation in a basal metazoan. Mol. Biol. Evol. 33, 2285–2293 (2016).

    CAS  Google Scholar 

  39. Klosin, A. & Lehner, B. Mechanisms, timescales and principles of trans-generational epigenetic inheritance in animals. Curr. Opin. Genet. Dev. 36, 41–49 (2016).

    CAS  Google Scholar 

  40. Holoch, D. & Moazed, D. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16, 71–84 (2015).

    CAS  Google Scholar 

  41. Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295–304 (2009).

    Article  CAS  Google Scholar 

  42. Rey, O., Danchin, E., Mirouze, M., Loot, C. & Blanchet, S. Adaptation to global change: a transposable element–epigenetics perspective. Trends Ecol. Evol. 31, 514–526 (2016).

    Google Scholar 

  43. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074–1080 (2001).

    CAS  Google Scholar 

  44. Karlić, R., Chung, H.-R., Lasserre, J., Vlahoviček, K. & Vingron, M. Histone modification levels are predictive for gene expression. Proc. Natl Acad. Sci. USA 107, 2926–2931 (2010).

    Google Scholar 

  45. Hamdoun, A. & Epel, D. Embryo stability and vulnerability in an always changing world. Proc. Natl Acad. Sci. USA 104, 1745–1750 (2007).

    CAS  Google Scholar 

  46. Wallace, D. C. & Fan, W. Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10, 12–31 (2010).

    CAS  Google Scholar 

  47. Marden, J. H. Nature's inordinate fondness for metabolic enzymes: why metabolic enzyme loci are so frequently targets of selection. Mol. Ecol. 22, 5743–5764 (2013).

    CAS  Google Scholar 

  48. Shaughnessy, D. T. et al. Mitochondria, energetics, epigenetics, and cellular responses to stress. Environ. Health Perspect. 122, 1271 (2014).

    CAS  Google Scholar 

  49. Gibbin, E. M. et al. Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan? J. Exp. Biol. 220, 551–563 (2017).

    Google Scholar 

  50. Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).

    CAS  Google Scholar 

  51. Willis, B. L. Phenotypic plasticity versus phenotypic stability in the reef corals Turbinaria mesenterina and Pavona cactus. Proc. Fifth Int. Coral Reef Symp. 4, 107–112 (1985).

    Google Scholar 

  52. Kenkel, C. D. & Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1, 0014 (2016).

    Google Scholar 

  53. Burton, T. & Metcalfe, N. B. Can environmental conditions experienced in early life influence future generations? Proc. R. Soc. B 281, 20140311 (2014).

    Google Scholar 

  54. Burgess, S. C. & Marshall, D. J. Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123, 769–776 (2014).

    Google Scholar 

  55. Galloway, L. F. & Etterson, J. R. Transgenerational plasticity is adaptive in the wild. Science 318, 1134–1136 (2007).

    CAS  Google Scholar 

  56. Baird, A. H., Guest, J. R. & Willis, B. L. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Ann. Rev. Ecol. Evol. Syst. 40, 551–571 (2009).

    Google Scholar 

  57. Richmond, R. H. Competency and dispersal potential of planula larvae of a spawning versus a brooding coral. In Proc. 6th Int. Coral Reef Symp. 2, 827–831 (1988).

    Google Scholar 

  58. Crean, A. J. & Marshall, D. J. Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos. Trans. R. Soc. B 364, 1087–1096 (2009).

    Google Scholar 

  59. Padilla-Gamiño, J. L., Pochon, X., Bird, C., Concepcion, G. T. & Gates, R. D. From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS One 7, e38440 (2012).

    Google Scholar 

  60. Highsmith, R. C. Reproduction by fragmentation in corals. Mar. Ecol. Prog. Ser. 7, 207–226 (1982).

    Google Scholar 

  61. Ayre, D. J. & Resing, J. M. Sexual and asexual production of planulae in reef corals. Mar. Biol. 90, 187–190 (1986).

    Google Scholar 

  62. Devlin-Durante, M. K. & Miller, M. W., Caribbean Acropora Research Group, Precht, W. F. & Baums, I. B. How old are you? Genet age estimates in a clonal animal. Mol. Ecol. 25, 5628–5646 (2016).

    CAS  Google Scholar 

  63. Reusch, T. B. H. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Evol. Appl. 7, 104–122 (2014).

    Google Scholar 

  64. Hall, V. R. & Hughes, T. P. Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77, 950–963 (1996).

    Google Scholar 

  65. Barfield, S., Aglyamova, G. V. & Matz, M. V. Evolutionary origins of germline segregation in Metazoa: evidence for a germ stem cell lineage in the coral Orbicella faveolata (Cnidaria, Anthozoa). Proc. R. Soc. B 283, 20152128 (2016).

    Google Scholar 

  66. Schweinsberg, M., Pech, R. A. G., Tollrian, R. & Lampert, K. P. Transfer of intracolonial genetic variability through gametes in Acropora hyacinthus corals. Coral Reefs 33, 77–87 (2013).

    Google Scholar 

  67. Rohwer, F. et al. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243, 1–10 (2002).

    Google Scholar 

  68. Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

    CAS  Google Scholar 

  69. Douglas, A. E. & Werren, J. H. Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7, e02099-15 (2016).

    Google Scholar 

  70. Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. H. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Change Biol. http://dx.doi.org/10.1111/gcb.13702 (2017). Experimental demonstration of rapid genetic adaptation of Symbiodinium to increased water temperatures.

  71. van Oppen, M. J., Baker, A. C., Coffroth, M. A. & Willis, B. L. In Coral Bleaching 83–102 (Springer, 2009).

    Google Scholar 

  72. Rowan, R. Review—diversity and ecology of zooxanthellae on coral reefs. J. Phycol. 34, 407–417 (1998).

    Google Scholar 

  73. Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Change 2, 116–120 (2012).

    Google Scholar 

  74. Hume, B. C. C. et al. 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 (2016).

    CAS  Google Scholar 

  75. Poland, D. M. & Coffroth, M. A. Trans-generational specificity within a cnidarian–algal symbiosis. Coral Reefs 36, 119–129 (2017).

    Google Scholar 

  76. Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B 275, 1359–1365 (2008).

    CAS  Google Scholar 

  77. Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. 105, 629–640 (2016).

    CAS  Google Scholar 

  78. Howells, E. J., Abrego, D., Meyer, E., Kirk, N. L. & Burt, J. A. Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob. Change Biol. 22, 2702–2714 (2016). Demonstration of the role of Symbiodinium community composition on corals' thermal tolerance.

    Google Scholar 

  79. Quigley, K. M., Willis, B. L. & Bay, L. K. Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis. R. Soc. Open Sci. 3, 160471 (2016).

    Google Scholar 

  80. Sharp, K. H., Distel, D. & Paul, V. J. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 6, 790–801 (2012).

    CAS  Google Scholar 

  81. Quigley, K. M. et al. Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One 9, e94297 (2014).

    Google Scholar 

  82. Lee, M. J. et al. Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb. Ecol. 71, 771–783 (2016).

    Google Scholar 

  83. Bay, L. K., Doyle, J., Logan, M. & Berkelmans, R. Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. R. Soc. Open Sci. 3, 160322 (2016).

    Google Scholar 

  84. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236 (2013).

    CAS  Google Scholar 

  85. Ainsworth, T. D. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261–2274 (2015).

    CAS  Google Scholar 

  86. Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 11, 186–200 (2017).

    Google Scholar 

  87. Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).

    CAS  Google Scholar 

  88. Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio 7, e00560-16 (2016).

    Google Scholar 

  89. Röthig, T., Yum, L. K., Kremb, S. G., Roik, A. & Voolstra, C. R. Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment. Sci. Rep. 7, 44714 (2017).

    Google Scholar 

  90. Casadesús, J. & Low, D. A. Programmed heterogeneity: epigenetic mechanisms in bacteria. J. Biol. Chem. 288, 13929–13935 (2013).

    Google Scholar 

  91. Celluzzi, A. & Masotti, A. How our other genome controls our epi-genome. Trends Microbiol. 24, 777–787 (2016).

    CAS  Google Scholar 

  92. Roossinck, M. J. The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol. 9, 99–108 (2011).

    CAS  Google Scholar 

  93. Shui, J.-W. et al. HVEM signalling at mucosal barriers provides host defence against pathogenic bacteria. Nature 488, 222–225 (2012).

    CAS  Google Scholar 

  94. Barr, J. J., Youle, M. & Rohwer, F. Innate and acquired bacteriophage-mediated immunity. Bacteriophage 3, e25857 (2013).

    Google Scholar 

  95. Rohwer, F. & Vega Thurber, R. L. Viruses manipulate the marine environment. Nature 459, 207–212 (2009).

    CAS  Google Scholar 

  96. Vega Thurber, R. L., Payet, J. P., Thurber, A. R. & Correa, A. M. S. Virus-host interactions and their roles in coral reef health and disease. Nat. Rev. Microbiol. 15, 205–216 (2017). Seminal review of the role of viruses in the phenotypic performance of the coral holobiont.

    Google Scholar 

  97. Raina, J. B. et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502, 677–680 (2013).

    CAS  Google Scholar 

  98. Correa, A. M. S. et al. Viral outbreak in corals associated with an in situ bleaching event: atypical herpes-like viruses and a new megavirus infecting Symbiodinium. Front. Microbiol. 7, 127 (2016).

    Google Scholar 

  99. Levin, R. A., Voolstra, C. R., Weynberg, K. D. & van Oppen, M. J. H. Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J. 11, 808–812 (2017).

    CAS  Google Scholar 

  100. Soffer, N., Brandt, M. E., Correa, A. M., Smith, T. B. & Vega Thurber, R. L. Potential role of viruses in white plague coral disease. ISME J. 8, 271–283 (2014).

    CAS  Google Scholar 

  101. LaJeunesse, T. C., Lee, S. Y., Gil-Agudelo, D. L., Knowlton, N. & Jeong, H. J. Symbiodinium necroappetens sp. nov. (Dinophyceae): an opportunist 'zooxanthella' found in bleached and diseased tissues of Caribbean reef corals. Eur. J. Phycol. 50, 223–238 (2015).

    Google Scholar 

  102. Harvell, D. et al. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20, 172–195 (2007).

    Google Scholar 

  103. van Oppen, M. J. H., Leong, J. A. & Gates, R. D. Coral-virus interactions: a double-edged sword? Symbiosis 47, 1–8 (2009).

    Google Scholar 

  104. Sampayo, E. M. et al. Coral symbioses under prolonged environmental change: living near tolerance range limits. Sci. Rep. 6, 36271 (2016).

    CAS  Google Scholar 

  105. Sarda, S., Zeng, J., Hunt, B. G. & Yi, S. V. The evolution of invertebrate gene body methylation. Mol. Biol. Evol. 29, 1907–1916 (2012).

    CAS  Google Scholar 

  106. Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e00028-16 (2016).

    Google Scholar 

  107. Ghalambor, C. K. et al. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372–375 (2015).

    CAS  Google Scholar 

  108. Kronholm, I. & Collins, S. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25, 1856–1868 (2016).

    CAS  Google Scholar 

  109. Ancel, L. W. Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58, 307–319 (2000).

    CAS  Google Scholar 

  110. Marshall, D. J. Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89, 418–427 (2008).

    Google Scholar 

  111. Messer, P. W. & Petrov, D. A. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol. Evol. 28, 659–669 (2013). Review of mechanisms that produce soft selective sweeps, with a case for soft sweeps dominating rapid adaptation in many species.

    Google Scholar 

  112. Whiteley, A. R., Fitzpatrick, S. W., Funk, W. C. & Tallmon, D. A. Genetic rescue to the rescue. Trends Ecol. Evol. 30, 42–49 (2015).

    Google Scholar 

  113. Holeski, L. M., Jander, G. & Agrawal, A. A. Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 27, 618–626 (2012).

    Google Scholar 

  114. Parker, L. M. et al. Adult exposure influences offspring response to ocean acidification in oysters. Glob. Change Biol. 18, 82–92 (2012).

    Google Scholar 

Download references

Acknowledgements

We dedicate this paper to our close friend and colleague, Dr. Sylvain Foret, a leader in coral genomics and invertebrate epigenetics who passed away unexpectedly days before this paper was submitted. The workshop where this paper was conceived was organized and funded by the ARC Centre of Excellence for Coral Reef Studies with additional support from the King Abdullah University of Science and Technology (KAUST) (M.A., M.L.B., T.R. and C.R.V.) and the KAUST Office of Competitive Research Funds award OCRF-2016-CRG4-25410101 (T.R. and M.L.B.). The authors would like to thank Xavier Pita for his help with Figs 1, 2, 3, Heno Hwang for his help with the figure in Box 1, and Hillary Smith for her help with Figs 2 and 3.

Author information

Authors and Affiliations

Authors

Contributions

This paper is the result of a workshop organized by G.T., P.L.M., B.L.W. and J.M.D. All co-authors contributed to discussions. G.T. wrote the first draft of the manuscript with input from J.M.D., B.L.W. and P.L.M. All co-authors contributed to subsequent drafts. Figures conceived and designed by: Fig. 1, J.M.D; Fig. 2, H.P.; Fig. 3, L.B., D.G.B., R.V.T., C.R.V., S.-A.W. and B.L.W. Box 1 was written by M.V.M., Box 2 by P.L.M. The figure in Box 1 was conceived and designed by M.V.M.

Corresponding author

Correspondence to Gergely Torda.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Torda, G., Donelson, J., Aranda, M. et al. Rapid adaptive responses to climate change in corals. Nature Clim Change 7, 627–636 (2017). https://doi.org/10.1038/nclimate3374

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nclimate3374

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing