Morphological stasis masks ecologically divergent coral species on tropical reefs

Pim Bongaerts; Ira R. Cooke; Hua Ying; Dagmar Wels; Stijn den Haan; Alejandra Hernandez-Agreda; Christopher A. Brunner; Sophie Dove; Norbert Englebert; Gal Eyal; Sylvain Forêt; Mila Grinblat; Kyra B. Hay; Saki Harii; David C. Hayward; Yu Lin; Morana Mihaljević; Aurelie Moya; Paul Muir; Frederic Sinniger; Patrick Smallhorn-West; Gergely Torda; Mark A. Ragan; Madeleine J.H. van Oppen; Ove Hoegh-Guldberg

doi:10.1016/j.cub.2021.03.028

Morphological stasis masks ecologically divergent coral species on tropical reefs

Pim Bongaerts
, Ira R. Cooke
, Hua Ying
, Dagmar Wels
, Stijn den Haan
, Alejandra Hernandez-Agreda
, Christopher A. Brunner
, Sophie Dove
, Norbert Englebert
, Gal Eyal
, Sylvain Forêt
, Mila Grinblat
, Kyra B. Hay
, Saki Harii
, David C. Hayward
, Yu Lin
, Morana Mihaljević
, Aurelie Moya
, Paul Muir
, Frederic Sinniger

Patrick Smallhorn-West, Gergely Torda, Mark A. Ragan, Madeleine J.H. van Oppen, Ove Hoegh-Guldberg

The Mina and Everard Goodman Faculty of Life Sciences - at Bar-Ilan University

California Academy of Sciences
University of Queensland
James Cook University Queensland
Australian National University
Central European University
Australian Institute of Marine Science
University of the Ryukyus
University of Zurich
University of Konstanz
Queensland Museum
University of Melbourne

Research output: Contribution to journal › Article › peer-review

76 Scopus citations

Abstract

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

Original language	English
Pages (from-to)	2286-2298.e8
Journal	Current Biology
Volume	31
Issue number	11
DOIs	https://doi.org/10.1016/j.cub.2021.03.028
State	Published - 7 Jun 2021

Bibliographical note

Publisher Copyright:
© 2021 The Author(s)

Funding

We thank David Whillas, Jaap Barendrecht, David Harris, Sara Naylor, and Annamieke van den Heuvel for support in the field or in the lab, as well as Underwater Earth, The Ocean Agency, and crews from Reef Connections, Mike Ball Dive Expeditions, SY Ethereal, and the Waitt Foundation. The authors acknowledge the Reef Future Genomics (ReFuGe) 2020 Consortium, of which this study was part, as organized by the Great Barrier Reef Foundation. This project was supported (in chronological order) by the XL Catlin Seaview Survey (2012–2014; funded by the XL Catlin Group in partnership with Underwater Earth and The University of Queensland), an Accelerate Partnerships grant from the Department of Science Information Technology Innovation and the Arts of the Queensland Government (2014–2016), an Australian Research Council Discovery Early Career Researcher Award (2016–2018; DE160101433 awarded to P.B.), and the Hope for Reefs Initiative at the California Academy of Sciences (2018–2020). Additional support was received from the Australian Research Council Centre for Excellence in Coral Reef Studies at The University of Queensland (awarded to O.H.-G.) and through a Natural Sciences grant no. 24133 from the Mitsubishi Foundation (awarded to S.H.). Substantial sea time was generously provided by the Waitt Foundation and the Joy Foundation. The genome assembly and whole-genome sequencing was funded by the Great Barrier Reef Foundation “Resilient Coral Reefs Successfully Adapting to Climate Change” program in collaboration with the Australian Government, Bioplatforms Australia through the National Collaborative Research Infrastructure Strategy, Rio Tinto, and a family foundation. P.B. I.R.C. H.Y. D.W. S.d.H. M.A.R. M.J.H.v.O. and O.H.-G. conceived and designed the research. P.B. D.W. S.d.H. C.A.B. S.D. N.E. G.E. M.G. K.B.H. D.C.H. M.M. P.M. and G.T. contributed to lab work. P.B. N.E. G.E. K.B.H. S.H. A.M. F.S. P.S.-W. and G.T. contributed to specimen collections. P.B. I.R.C. H.Y. D.W. S.d.H. A.H.-A. S.F. and Y.L. contributed to analyses. P.B. wrote the paper, and all authors contributed manuscript edits. The authors declare no competing interests. We thank David Whillas, Jaap Barendrecht, David Harris, Sara Naylor, and Annamieke van den Heuvel for support in the field or in the lab, as well as Underwater Earth, The Ocean Agency, and crews from Reef Connections, Mike Ball Dive Expeditions, SY Ethereal, and the Waitt Foundation. The authors acknowledge the Reef Future Genomics (ReFuGe) 2020 Consortium, of which this study was part, as organized by the Great Barrier Reef Foundation. This project was supported (in chronological order) by the XL Catlin Seaview Survey (2012–2014; funded by the XL Catlin Group in partnership with Underwater Earth and The University of Queensland ), an Accelerate Partnerships grant from the Department of Science Information Technology Innovation and the Arts of the Queensland Government (2014–2016), an Australian Research Council Discovery Early Career Researcher Award (2016–2018; DE160101433 awarded to P.B.), and the Hope for Reefs Initiative at the California Academy of Sciences (2018–2020). Additional support was received from the Australian Research Council Centre for Excellence in Coral Reef Studies at The University of Queensland (awarded to O.H.-G.) and through a Natural Sciences grant no. 24133 from the Mitsubishi Foundation (awarded to S.H.). Substantial sea time was generously provided by the Waitt Foundation and the Joy Foundation. The genome assembly and whole-genome sequencing was funded by the Great Barrier Reef Foundation “Resilient Coral Reefs Successfully Adapting to Climate Change” program in collaboration with the Australian Government , Bioplatforms Australia through the National Collaborative Research Infrastructure Strategy , Rio Tinto , and a family foundation.

Funders	Funder number
Bioplatforms Australia
Hope for Reefs Initiative
Ocean Agency
XL Catlin Seaview Survey
family foundation
Joyce Foundation
Waitt Foundation
Great Barrier Reef Foundation
California Academy of Sciences	24133
Australian Research Council	DE160101433
University of Queensland
Mitsubishi Foundation
Department of Science, Information Technology and Innovation, Queensland Government

Keywords

Pachyseris
Scleractinia
coral reefs
cryptic diversity
mesophotic
nuclear genome

Access to Document

10.1016/j.cub.2021.03.028

Cite this

Bongaerts, P., Cooke, I. R., Ying, H., Wels, D., den Haan, S., Hernandez-Agreda, A., Brunner, C. A., Dove, S., Englebert, N., Eyal, G., Forêt, S., Grinblat, M., Hay, K. B., Harii, S., Hayward, D. C., Lin, Y., Mihaljević, M., Moya, A., Muir, P., ... Hoegh-Guldberg, O. (2021). Morphological stasis masks ecologically divergent coral species on tropical reefs. Current Biology, 31(11), 2286-2298.e8. https://doi.org/10.1016/j.cub.2021.03.028

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title = "Morphological stasis masks ecologically divergent coral species on tropical reefs",

abstract = "Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.",

keywords = "Pachyseris, Scleractinia, coral reefs, cryptic diversity, mesophotic, nuclear genome",

author = "Pim Bongaerts and Cooke, \{Ira R.\} and Hua Ying and Dagmar Wels and \{den Haan\}, Stijn and Alejandra Hernandez-Agreda and Brunner, \{Christopher A.\} and Sophie Dove and Norbert Englebert and Gal Eyal and Sylvain For{\^e}t and Mila Grinblat and Hay, \{Kyra B.\} and Saki Harii and Hayward, \{David C.\} and Yu Lin and Morana Mihaljevi{\'c} and Aurelie Moya and Paul Muir and Frederic Sinniger and Patrick Smallhorn-West and Gergely Torda and Ragan, \{Mark A.\} and \{van Oppen\}, \{Madeleine J.H.\} and Ove Hoegh-Guldberg",

note = "Publisher Copyright: {\textcopyright} 2021 The Author(s)",

year = "2021",

month = jun,

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doi = "10.1016/j.cub.2021.03.028",

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Bongaerts, P, Cooke, IR, Ying, H, Wels, D, den Haan, S, Hernandez-Agreda, A, Brunner, CA, Dove, S, Englebert, N, Eyal, G, Forêt, S, Grinblat, M, Hay, KB, Harii, S, Hayward, DC, Lin, Y, Mihaljević, M, Moya, A, Muir, P, Sinniger, F, Smallhorn-West, P, Torda, G, Ragan, MA, van Oppen, MJH & Hoegh-Guldberg, O 2021, 'Morphological stasis masks ecologically divergent coral species on tropical reefs', Current Biology, vol. 31, no. 11, pp. 2286-2298.e8. https://doi.org/10.1016/j.cub.2021.03.028

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AU - Bongaerts, Pim

AU - Cooke, Ira R.

AU - Ying, Hua

AU - Wels, Dagmar

AU - den Haan, Stijn

AU - Hernandez-Agreda, Alejandra

AU - Brunner, Christopher A.

AU - Dove, Sophie

AU - Englebert, Norbert

AU - Eyal, Gal

AU - Forêt, Sylvain

AU - Grinblat, Mila

AU - Hay, Kyra B.

AU - Harii, Saki

AU - Hayward, David C.

AU - Lin, Yu

AU - Mihaljević, Morana

AU - Moya, Aurelie

AU - Muir, Paul

AU - Sinniger, Frederic

AU - Smallhorn-West, Patrick

AU - Torda, Gergely

AU - Ragan, Mark A.

AU - van Oppen, Madeleine J.H.

AU - Hoegh-Guldberg, Ove

PY - 2021/6/7

Y1 - 2021/6/7

N2 - Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

AB - Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

KW - Pachyseris

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KW - coral reefs

KW - cryptic diversity

KW - mesophotic

KW - nuclear genome

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ER -

Morphological stasis masks ecologically divergent coral species on tropical reefs

Abstract

Bibliographical note

Funding

Keywords

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