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.
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Code is included on figshare https://doi.org/10.6084/m9.figshare.12363953.
IPCC Climate Change 2007: The Physical Science Basis (eds Solomon S. et al.) (Cambridge Univ. Press, 2007).
Kleypas, J. A. et al. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 (1999).
De’ath, G., Lough, J. M. & Fabricius, K. E. Declining coral calcification on the Great Barrier Reef. Science 323, 116–119 (2009).
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).
Kleypas, J. A. & Yates, K. K. Coral reefs and ocean acidification. Oceanography 22, 108–117 (2009).
Eyre, B. D. et al. Coral reefs will transition to net dissolving before end of century. Science 359, 908–911 (2018).
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).
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).
Balthasar, U. & Cusack, M. Aragonite-calcite seas—quantifying the gray area. Geology 43, 99–102 (2015).
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).
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).
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).
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).
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).
Suggett, D. J. et al. Sea anemones may thrive in a high CO2 world. Glob. Change Biol. 18, 3015–3025 (2012).
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).
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).
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).
Zapata, F. et al. Phylogenomic analyses support traditional relationships within Cnidaria. PLoS ONE 10, e0139068 (2015).
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).
Xiao, M. et al. Mitogenomics suggests a sister relationship of Relicanthus daphneae (Cnidaria: Anthozoa: Hexacorallia: incerti ordinis) with Actiniaria. Sci. Rep. 9, 18182 (2019).
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).
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).
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).
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).
Gabay, Y., Fine, M., Barkay, Z. & Benayahu, Y. Octocoral tissue provides protection from declining oceanic pH. PLoS ONE 9, e91553 (2014).
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).
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).
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).
Drake, J. L. et al. How corals made rocks through the ages. Glob. Change Biol. 26, 31 (2019).
Tambutté, S. et al. Coral biomineralization: from the gene to the environment. J. Exp. Mar. Biol. Ecol. 408, 58–78 (2011).
Sevilgen, D. S. et al. Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci. Adv. 5, eaau7447 (2019).
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).
Higuchi, T. et al. Biotic control of skeletal growth by scleractinian corals in aragonite–calcite seas. PLoS ONE 9, e91021 (2014).
Prada, C. et al. Empty niches after extinctions increase population sizes of modern corals. Curr. Biol. 26, 3190–3194 (2016).
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).
Kiessling, W. & Aberhan, M. Environmental determinants of marine benthic biodiversity dynamics through Triassic–Jurassic time. Paleobiology 33, 414–434 (2007).
Richards, Z. T. et al. Integrated evidence reveals a new species in the ancient blue coral genus Heliopora (Octocorallia). Sci. Rep. 8, 15875 (2018).
Bhattacharya, D. et al. Comparative genomics explains the evolutionary success of reef-forming corals. eLife 5, e13288 (2016).
Squires, D. F. The evolution of the deep-sea coral family Micrabaciidae. Stud. Trop. Oceanogr. 5, 502–510 (1967).
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).
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).
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).
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 https://www.biorxiv.org/content/10.1101/2020.02.25.965517v1 (2020).
Faircloth, B. C. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32, 786–788 (2016).
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
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).
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).
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).
Mai, U. & Mirarab, S. TreeShrink: fast and accurate detection of outlier long branches in collections of phylogenetic trees. BMC Genom. 19, 272 (2018).
Junier, T. & Zdobnov, E. M. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 26, 1669–1670 (2010).
Bouckaert, R. et al. BEAST2 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).
Ho, S. Y. & Phillips, M. J. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 58, 367–380 (2009).
Stolarski, J. et al. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol. Biol. 11, 316 (2011).
Oliveros, C. H. et al. Earth history and the passerine superradiation. Proc. Natl Acad. Sci. USA 116, 7916–7925 (2019).
Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002).
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).
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).
Brown, J. W. & Smith, S. A. The past sure is tense: on interpreting phylogenetic divergence time estimates. Syst. Biol. 67, 340–353 (2018).
Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
Höhna, S. et al. RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst. Biol. 65, 726–736 (2016).
Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).
Höhna S. et al. Bayesian approach for estimating branch-specific speciation and extinction rates. Preprint at bioRxiv https://doi.org/10.1101/555805 (2019).
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.
The authors declare no competing interests
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.
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.
BEAST2 dated phylogeny with 95% highest posterior densities (blue bars) of node ages and red circles to denote fossil calibration points.
ASTRAL III species tree with posterior probabilities calculated in ASTRAL.
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).
Number of loci recovered for each species in anthozoan sub-classes and class Medusozoa. *=loci extracted from genomes.
About this article
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). https://doi.org/10.1038/s41559-020-01291-1
Coral Reefs (2021)
Unusual shallow water Devonian coral community from Queensland and its recent analogues from the inshore Great Barrier Reef
Coral Reefs (2021)
Unexpected high abundance of aragonite-forming Nanipora (Octocorallia: Helioporacea) at an acidified volcanic reef in southern Japan
Marine Biodiversity (2021)
Palaeobiodiversity and Palaeoenvironments (2021)
Marine Biodiversity (2021)