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

Nature Ecology & Evolution volume 4, pages 1531–1538 (2020)Cite this article

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Abstract

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.

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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 https://doi.org/10.5061/dryad.36n40. Alignment and tree files, BEAST2 xml and result files: figshare https://doi.org/10.6084/m9.figshare.12363953.

Code availability

Code is included on figshare https://doi.org/10.6084/m9.figshare.12363953.

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Acknowledgements

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

Authors and Affiliations

  1. Biology Department, Harvey Mudd College, Claremont, CA, USA

    Andrea M. Quattrini & Catherine S. McFadden

  2. Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC, USA

    Andrea M. Quattrini

  3. Division of Invertebrate Zoology, American Museum of Natural History, New York, NY, USA

    Estefanía Rodríguez & Mercer R. Brugler

  4. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA

    Brant C. Faircloth & Michael E. Hellberg

  5. Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA

    Brant C. Faircloth

  6. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

    Peter F. Cowman

  7. Department of Natural Sciences, University of South Carolina Beaufort, Beaufort, SC, USA

    Mercer R. Brugler

  8. Department of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington DC, USA

    Gabriela A. Farfan

  9. Institute of Marine Science, Federal University of São Paulo, Santos, Brazil

    Marcelo V. Kitahara

  10. Centre for Marine Biology, University of São Paulo, São Sebastião, Brazil

    Marcelo V. Kitahara

  11. US Geological Survey, Leetown Science Center, Kearneysville, WV, USA

    Cheryl L. Morrison

  12. CONACyT-Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Laboratorio de Necton y Ecología de Arrecifes, La Paz, México

    David A. Paz-García

  13. Molecular Invertebrate Systematics and Ecology Laboratory, Department of Marine Science, Chemistry, and Biology, Faculty of Science, University of the Ryukyus, Nishihara, Japan

    James D. Reimer

  14. Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Japan

    James D. Reimer

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  1. Andrea M. Quattrini
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  2. Estefanía Rodríguez
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Contributions

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.

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Correspondence to Andrea M. Quattrini.

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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.

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Supplementary Tables 2 and 3.

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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

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