Skip to main content

Thank you for visiting 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.

Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time


Identifying how past environmental conditions shaped the evolution of corals and their skeletal traits provides a framework for predicting their persistence and that of their non-calcifying relatives under impending global warming and ocean acidification. Here we show that ocean geochemistry, particularly aragonite–calcite seas, drives patterns of morphological evolution in anthozoans (corals, sea anemones) by examining skeletal traits in the context of a robust, time-calibrated phylogeny. The lability of skeletal composition among octocorals suggests a greater ability to adapt to changes in ocean chemistry compared with the homogeneity of the aragonitic skeleton of scleractinian corals. Pulses of diversification in anthozoans follow mass extinctions and reef crises, with sea anemones and proteinaceous corals filling empty niches as tropical reef builders went extinct. Changing environmental conditions will likely diminish aragonitic reef-building scleractinians, but the evolutionary history of the Anthozoa suggests other groups will persist and diversify in their wake.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Phylogeny of Anthozoa with ancestral character states of skeletal types.
Fig. 2: Timing and origin of anthozoans and their skeletal features across time and palaeoclimate ocean conditions.
Fig. 3: Branch-specific diversification rates across Anthozoa.

Data availability

Raw data: NCBI Genbank BioProject# PRJNA413622 and PRJNA588468, BioSample #SAMN07774920-4952, 13244867-5050. Anthozoan bait set: Data Dryad Entry Alignment and tree files, BEAST2 xml and result files: figshare

Code availability

Code is included on figshare


  1. 1.

    IPCC Climate Change 2007: The Physical Science Basis (eds Solomon S. et al.) (Cambridge Univ. Press, 2007).

  2. 2.

    Kleypas, J. A. et al. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 (1999).

    CAS  Article  Google Scholar 

  3. 3.

    De’ath, G., Lough, J. M. & Fabricius, K. E. Declining coral calcification on the Great Barrier Reef. Science 323, 116–119 (2009).

    Article  CAS  Google Scholar 

  4. 4.

    Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M. & McCorkle, D. C. Ocean warming slows coral growth in the central Red Sea. Science 329, 322–325 (2010).

    CAS  Article  Google Scholar 

  5. 5.

    Kleypas, J. A. & Yates, K. K. Coral reefs and ocean acidification. Oceanography 22, 108–117 (2009).

    Article  Google Scholar 

  6. 6.

    Eyre, B. D. et al. Coral reefs will transition to net dissolving before end of century. Science 359, 908–911 (2018).

    CAS  Article  Google Scholar 

  7. 7.

    Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008).

    CAS  Article  Google Scholar 

  8. 8.

    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  Article  Google Scholar 

  9. 9.

    Balthasar, U. & Cusack, M. Aragonite-calcite seas—quantifying the gray area. Geology 43, 99–102 (2015).

    CAS  Article  Google Scholar 

  10. 10.

    De Choudens-Sanchez, V. & Gonzalez, L. A. Calcite and aragonite precipitation under controlled instantaneous supersaturation: elucidating the role of CaCO3 saturation state and Mg/Ca ratio on calcium carbonate polymorphism. J. Sediment. Res. 79, 363–376 (2009).

    Article  CAS  Google Scholar 

  11. 11.

    Ries, J. B. Geological and experimental evidence for secular variation in seawater Mg/Ca (calcite–aragonite seas) and its effects on marine biological calcification. Biogeosciences 7, 2795–2849 (2010).

    CAS  Article  Google Scholar 

  12. 12.

    Kiessling, W. & Simpson, C. On the potential for ocean acidification to be a general cause of ancient reef crises. Glob. Change Biol. 17, 56–67 (2011).

    Article  Google Scholar 

  13. 13.

    Morse, J. W., Mucci, A. & Millero, F. J. The solubility of calcite and aragonite in seawater of 35% salinity at 25°C and atmospheric pressure. Geochim. Cosmochim. Acta 44, 85–94 (1980).

    CAS  Article  Google Scholar 

  14. 14.

    Morse, J. W., Andersson, A. J. & Mackenzie, F. T. Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and “ocean acidification”: role of high Mg-calcites. Geochim. Cosmochim. Acta 23, 5814–5830 (2006).

    Article  CAS  Google Scholar 

  15. 15.

    Suggett, D. J. et al. Sea anemones may thrive in a high CO2 world. Glob. Change Biol. 18, 3015–3025 (2012).

    Article  Google Scholar 

  16. 16.

    Tsounis, G. & Edmunds, P. J. Three decades of coral reef community dynamics in St. John, USVI: a contrast of scleractinians and octocorals. Ecosphere 8, e01646 (2017).

    Article  Google Scholar 

  17. 17.

    Tkachenko, K. S., Wu, B. J., Fang, L. S. & Fan, T. Y. Dynamics of a coral reef community after mass mortality of branching Acropora corals and an outbreak of anemones. Mar. Biol. 151, 185–194 (2007).

    Article  Google Scholar 

  18. 18.

    Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Change 3, 683–687 (2013).

    CAS  Article  Google Scholar 

  19. 19.

    Zapata, F. et al. Phylogenomic analyses support traditional relationships within Cnidaria. PLoS ONE 10, e0139068 (2015).

    Article  CAS  Google Scholar 

  20. 20.

    Kayal, E. et al. Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits. BMC Evol. Biol. 18, 68 (2018).

    Article  CAS  Google Scholar 

  21. 21.

    Xiao, M. et al. Mitogenomics suggests a sister relationship of Relicanthus daphneae (Cnidaria: Anthozoa: Hexacorallia: incerti ordinis) with Actiniaria. Sci. Rep. 9, 18182 (2019).

    CAS  Article  Google Scholar 

  22. 22.

    McFadden, C. S., France, S. C., Sánchez, J. A. & Alderslade, P. A. Molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol. Phylogenet. Evol. 41, 513–527 (2006).

    CAS  Article  Google Scholar 

  23. 23.

    Berntson, E. A., Bayer, F. M., McArthur, A. G. & France, S. C. Phylogenetic relationships within the Octocorallia (Cnidaria: Anthozoa) based on nuclear 18S rRNA sequences. Mar. Biol. 138, 235–246 (2001).

    CAS  Article  Google Scholar 

  24. 24.

    Medina, M., Collins, A. G., Takaoka, T. L., Kuehl, J. V. & Boore, J. L. Naked corals: skeleton loss in Scleractinia. Proc. Natl Acad. Sci. USA 103, 9096–9100 (2006).

    CAS  Article  Google Scholar 

  25. 25.

    Bayer, F. M. & Macintyre, I. G. The mineral component of the axis and holdfast of some gorgonacean octocorals (Coelenteratea: Anthozoa), with special reference to the family Gorgoniidae. Proc. Biol. Soc. 103, 205–228 (2001).

    Google Scholar 

  26. 26.

    Gabay, Y., Fine, M., Barkay, Z. & Benayahu, Y. Octocoral tissue provides protection from declining oceanic pH. PLoS ONE 9, e91553 (2014).

    Article  CAS  Google Scholar 

  27. 27.

    Purgstaller, B., Mavromatis, V., Immenhauser, A. & Dietzel, M. Transformation of Mg-bearing amorphous calcium carbonate to Mg-calcite—in situ monitoring. Geochim. Cosmochim. Acta 174, 180–195 (2016).

    CAS  Article  Google Scholar 

  28. 28.

    Ries, J. B. Effect of ambient Mg/Ca ratio on Mg fractionation in calcareous marine invertebrates: a record of the oceanic Mg/Ca ratio over the Phanerozoic. Geology 32, 981–984 (2004).

    CAS  Article  Google Scholar 

  29. 29.

    Conci, N., Wörheide, G. & Vargas, S. New non-bilaterian transcriptomes provide novel insights into the evolution of coral skeletomes. Genome Biol. Evol. 11, 3068–3081 (2019).

    CAS  Article  Google Scholar 

  30. 30.

    Drake, J. L. et al. How corals made rocks through the ages. Glob. Change Biol. 26, 31 (2019).

    Article  Google Scholar 

  31. 31.

    Tambutté, S. et al. Coral biomineralization: from the gene to the environment. J. Exp. Mar. Biol. Ecol. 408, 58–78 (2011).

    Article  Google Scholar 

  32. 32.

    Sevilgen, D. S. et al. Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci. Adv. 5, eaau7447 (2019).

    Article  CAS  Google Scholar 

  33. 33.

    Higuchi, T., Shirai, K., Mezaki, T. & Yuyama, I. Temperature dependence of aragonite and calcite skeleton formation by a scleractinian coral in low mMg/Ca seawater. Geology 45, 1087–1090 (2017).

    Article  Google Scholar 

  34. 34.

    Higuchi, T. et al. Biotic control of skeletal growth by scleractinian corals in aragonite–calcite seas. PLoS ONE 9, e91021 (2014).

    Article  Google Scholar 

  35. 35.

    Prada, C. et al. Empty niches after extinctions increase population sizes of modern corals. Curr. Biol. 26, 3190–3194 (2016).

    CAS  Article  Google Scholar 

  36. 36.

    Stanley, G. D., Shepherd, H. M. E. & Robinson, A. J. Paleoecological response of corals to the end-triassic mass extinction: an integrational analysis. J. Int. Earth Sci. 29, 879–885 (2018).

    CAS  Article  Google Scholar 

  37. 37.

    Kiessling, W. & Aberhan, M. Environmental determinants of marine benthic biodiversity dynamics through Triassic–Jurassic time. Paleobiology 33, 414–434 (2007).

    Article  Google Scholar 

  38. 38.

    Richards, Z. T. et al. Integrated evidence reveals a new species in the ancient blue coral genus Heliopora (Octocorallia). Sci. Rep. 8, 15875 (2018).

    Article  CAS  Google Scholar 

  39. 39.

    Bhattacharya, D. et al. Comparative genomics explains the evolutionary success of reef-forming corals. eLife 5, e13288 (2016).

    Article  Google Scholar 

  40. 40.

    Squires, D. F. The evolution of the deep-sea coral family Micrabaciidae. Stud. Trop. Oceanogr. 5, 502–510 (1967).

    Google Scholar 

  41. 41.

    Guinotte, J. M. et al. Will human‐induced changes in seawater chemistry alter the distribution of deep‐sea scleractinian corals? Front. Ecol. Envir. 4, 141–146 (2006).

    Article  Google Scholar 

  42. 42.

    Edmunds, P. J. & Lasker, H. R. Cryptic regime shift in benthic community structure on shallow reefs in St. John, US Virgin Islands. Mar. Ecol. Prog. Ser. 559, 1–12 (2016).

    Article  Google Scholar 

  43. 43.

    Quattrini, A. M. et al. Universal target‐enrichment baits for anthozoan (Cnidaria) phylogenomics: new approaches to long‐standing problems. Mol. Ecol. Resour. 18, 281–295 (2018).

    CAS  Article  Google Scholar 

  44. 44.

    Cowman, P. F. et al. An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives. Preprint at bioRxiv (2020).

  45. 45.

    Faircloth, B. C. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32, 786–788 (2016).

    CAS  Article  Google Scholar 

  46. 46.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    CAS  Article  Google Scholar 

  47. 47.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  Article  Google Scholar 

  48. 48.

    Lanfear, R., Calcott, B., Ho, S. Y. W. & Guindon, S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701 (2012).

    CAS  Article  Google Scholar 

  49. 49.

    Aberer, A. J., Kobert, K. & Stamatakis, A. ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31, 2553–2556 (2014).

    CAS  Article  Google Scholar 

  50. 50.

    Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinform. 19, 153 (2018).

    Article  Google Scholar 

  51. 51.

    Mai, U. & Mirarab, S. TreeShrink: fast and accurate detection of outlier long branches in collections of phylogenetic trees. BMC Genom. 19, 272 (2018).

    Article  Google Scholar 

  52. 52.

    Junier, T. & Zdobnov, E. M. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 26, 1669–1670 (2010).

    CAS  Article  Google Scholar 

  53. 53.

    Bouckaert, R. et al. BEAST2 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).

    CAS  Article  Google Scholar 

  54. 54.

    Ho, S. Y. & Phillips, M. J. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 58, 367–380 (2009).

    Article  Google Scholar 

  55. 55.

    Stolarski, J. et al. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol. Biol. 11, 316 (2011).

    Article  Google Scholar 

  56. 56.

    Oliveros, C. H. et al. Earth history and the passerine superradiation. Proc. Natl Acad. Sci. USA 116, 7916–7925 (2019).

    CAS  Article  Google Scholar 

  57. 57.

    Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002).

    CAS  Article  Google Scholar 

  58. 58.

    Smith, S. A., Brown, J. W. & Walker, J. F. So many genes, so little time: a practical approach to divergence-time estimation in the genomic era. PLoS ONE 13, e0197433 (2018).

    Article  CAS  Google Scholar 

  59. 59.

    Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901 (2018).

    CAS  Article  Google Scholar 

  60. 60.

    Brown, J. W. & Smith, S. A. The past sure is tense: on interpreting phylogenetic divergence time estimates. Syst. Biol. 67, 340–353 (2018).

    Article  Google Scholar 

  61. 61.

    Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).

    Article  Google Scholar 

  62. 62.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  63. 63.

    Höhna, S. et al. RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst. Biol. 65, 726–736 (2016).

    Article  Google Scholar 

  64. 64.

    Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).

    CAS  Article  Google Scholar 

  65. 65.

    Höhna S. et al. Bayesian approach for estimating branch-specific speciation and extinction rates. Preprint at bioRxiv (2019).

Download references


NSF #1457817 and #1457581 provided funding to C.S.M. and E.R. and ARC DECRA (DE170100516) provided funding to P.F.C. A few specimens were collected during the R/V Atlantis DEEPSEARCH cruise (E. Cordes, chief scientist), which was funded by the US Department of the Interior, Bureau of Ocean Energy Management, Environmental Studies Program, Washington DC, under contract number M17PC00009 and on the R/V Celtic Explorer supported by the Marine Institute’s Shiptime Programme (L. Allcock, chief scientist). A. Pentico, F. Guitierrez, S. Goldman, S. Moaleman and M. Taylor helped with lab work. N. Bezio created outlined illustrations and A. Siqueira helped create the tip density plot. C. Oliveros, B. Smith and S. Ho provided guidance in divergence dating analyses. We thank A. Collins, L. Dueñas, D. Erwin, V. Gonzalez, G. Sahwell and S. Tweedt for helpful discussions and J. McCormack and W. Tsai for use of the sonicator at Occidental College. T. Bridge, M. Daly, M. Taylor, C. Prada and J. Sánchez provided specimens. Any use of trade, product or firm names is for descriptive purposes only and does not imply endorsement by the US Government.

Author information




C.S.M., E.R. and A.M.Q. conceived and designed this study. A.M.Q., C.S.M., E.R., M.R.B., M.E.H. and D.A.P.-G. conducted molecular lab work. A.M.Q. conducted bioinformatic and phylogenetic analyses with guidance from B.C.F. D.A.P.-G. and P.F.C. helped with figure preparation. A.M.Q., E.R. and C.S.M. wrote the manuscript. M.E.H. contributed improvements to the text. P.F.C. contributed text to the supplementary file. A.M.Q., E.R., B.C.F., P.F.C., M.R.B., G.A.F., M.V.K., M.E.H., C.L.M., D.A.P.-G., J.D.R. and C.S.M. aided in interpretation of results. All authors contributed to a draft of the manuscript and approved the final version of the manuscript.

Corresponding author

Correspondence to Andrea M. Quattrini.

Ethics declarations

Competing interests

The authors declare no competing interests

Additional information

Peer review information Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Photographs of anthozoans.

Acropora sp. (Scleractinia, stony coral), Javania sp. (Scleractinia, solitary stony coral), Corynactis annulata (Corallimorpharia, naked coral), Telopathes magna (Antipatharia, black coral); Hexacorals middle row, left to right: Relicanthus cf. daphneae (Actiniaria, anemone), Actiniidae sp. (Actiniaria, anemone), Zoanthus sansibaricus (Zoantharia, colonial anemone), Ceriantharia (Ceriantharia, tube anemone); Octocorals bottom row, left to right: Plexaurella nutans and Gorgonia ventalina (Alcyonacea, holaxonian gorgonians), Anthomastus sp. (Alcyonacea, soft coral), Keratoisidinae (Alcyonacea, calcaxonian gorgonian), Virgularia cf. gustaviana (Pennatulacea, sea pen). Photographs taken by C.S. McFadden, J. D. Reimer, or courtesy of NOAA Office of Ocean Exploration and Research.

Extended Data Fig. 2 Time-calibrated phylogeny.

BEAST2 dated phylogeny with 95% highest posterior densities (blue bars) of node ages and red circles to denote fossil calibration points.

Extended Data Fig. 3 Species tree.

ASTRAL III species tree with posterior probabilities calculated in ASTRAL.

Extended Data Fig. 4 Net diversification rates.

Net diversification rates (speciation minus extinction) across deep time. A) calculated between mass extinction events (solid lines) and reef crises (*), and B) between aragonite-calcite sea intervals (dotted lines).

Extended Data Fig. 5 Locus recovery per species.

Number of loci recovered for each species in anthozoan sub-classes and class Medusozoa. *=loci extracted from genomes.

Supplementary information

Supplementary Information

Results, discussion and Supplementary Tables 1, 4 and 5.

Reporting Summary

Peer Review Information

Supplementary Data

Supplementary Tables 2 and 3.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Quattrini, A.M., Rodríguez, E., Faircloth, B.C. et al. Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time. Nat Ecol Evol 4, 1531–1538 (2020).

Download citation

Further reading


Quick links