The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals
Symbiosis and coloniality are ecologically important traits for corals of the order Scleractinia. Symbiotic (zooxanthellate) species are highly successful in shallow waters of tropical and subtropical seas and most of them are colonial. On the other hand, azooxanthellate species present wide distrib...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-06-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmars.2020.00461/full |
| _version_ | 1831658027537661952 |
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| author | Ana Navarro Campoy Ana Navarro Campoy Anna Maria Addamo Anna Maria Addamo Annie Machordom Andrew Meade Marcelo M. Rivadeneira Marcelo M. Rivadeneira Marcelo M. Rivadeneira Cristián E. Hernández Cristián E. Hernández Chris Venditti |
| author_facet | Ana Navarro Campoy Ana Navarro Campoy Anna Maria Addamo Anna Maria Addamo Annie Machordom Andrew Meade Marcelo M. Rivadeneira Marcelo M. Rivadeneira Marcelo M. Rivadeneira Cristián E. Hernández Cristián E. Hernández Chris Venditti |
| author_sort | Ana Navarro Campoy |
| collection | DOAJ |
| description | Symbiosis and coloniality are ecologically important traits for corals of the order Scleractinia. Symbiotic (zooxanthellate) species are highly successful in shallow waters of tropical and subtropical seas and most of them are colonial. On the other hand, azooxanthellate species present wide distribution ranges and expand to the deep-sea at more than 6,000 m depth. These are mostly solitary, with only few species colonial that form extensive deep reefs. Each ecologically distinctive group encompasses half of the biodiversity of the order and they are not grouped into differentiated monophyletic clades. Paleontologists and evolutionary biologists have debated for decades whether modern scleractinian corals have evolved from symbiotic or colonial ancestors and how these traits have evolved and being involved in the diversification process in corals. Previous comparative analyses throw evidence in favor of coevolution of these characters and toward repetitive loss of symbiosis and coloniality. Nevertheless, the discovery of the origin of the group deep in the Paleozoic, with a deep divergent clade composed of only azooxanthellate corals has questioned these findings. With this work, we disentangle the patterns in the evolution of symbiosis and coloniality, testing if they are correlated and if they follow a gradual or episodic mode of evolution. To this end, we first produce the most complete time-calibrated phylogenetic tree for the order Scleractinia, including new sequences of never-before sampled species and genera. These novel sequences contribute to alleviate the current molecular under sampling of azooxanthellate species. Incorporating phylogenetic uncertainty, we obtained strong evidence in favor of a correlated and episodic model of evolution. This model led to the inference of an azooxanthellate and solitary most recent ancestor of scleractinians. Transition rates between the four different combinations of the two traits showed that while coloniality is gained and lost multiple times, symbiosis first appears around 282 Ma and is never lost. Also, coloniality seems to have appeared before symbiosis in azooxanthellate lineages. Thus, azooxanthellate corals, and especially colonial lineages, have been acting as a source of biodiversity for shallow zooxanthellate coral communities, highlighting the uniqueness of shallow and deep species and the need to preserve them. |
| first_indexed | 2024-12-19T17:37:33Z |
| format | Article |
| id | doaj.art-6912df7559ef4c9f890f7784afb8e62b |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-12-19T17:37:33Z |
| publishDate | 2020-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-6912df7559ef4c9f890f7784afb8e62b2022-12-21T20:12:17ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-06-01710.3389/fmars.2020.00461547691The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian CoralsAna Navarro Campoy0Ana Navarro Campoy1Anna Maria Addamo2Anna Maria Addamo3Annie Machordom4Andrew Meade5Marcelo M. Rivadeneira6Marcelo M. Rivadeneira7Marcelo M. Rivadeneira8Cristián E. Hernández9Cristián E. Hernández10Chris Venditti11Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, ChileCentro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, ChileDepartamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Madrid, SpainEuropean Commission, Joint Research Centre (JRC), Ispra, ItalyDepartamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Madrid, SpainThe School of Biological Sciences, University of Reading, Reading, United KingdomDepartamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, ChileCentro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, ChileDepartamento de Biología, Universidad de La Serena, La Serena, ChileLaboratorio de Ecología Evolutiva y Filoinformática, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, ChileUniversidad Católica de Santa María, Arequipa, PeruThe School of Biological Sciences, University of Reading, Reading, United KingdomSymbiosis and coloniality are ecologically important traits for corals of the order Scleractinia. Symbiotic (zooxanthellate) species are highly successful in shallow waters of tropical and subtropical seas and most of them are colonial. On the other hand, azooxanthellate species present wide distribution ranges and expand to the deep-sea at more than 6,000 m depth. These are mostly solitary, with only few species colonial that form extensive deep reefs. Each ecologically distinctive group encompasses half of the biodiversity of the order and they are not grouped into differentiated monophyletic clades. Paleontologists and evolutionary biologists have debated for decades whether modern scleractinian corals have evolved from symbiotic or colonial ancestors and how these traits have evolved and being involved in the diversification process in corals. Previous comparative analyses throw evidence in favor of coevolution of these characters and toward repetitive loss of symbiosis and coloniality. Nevertheless, the discovery of the origin of the group deep in the Paleozoic, with a deep divergent clade composed of only azooxanthellate corals has questioned these findings. With this work, we disentangle the patterns in the evolution of symbiosis and coloniality, testing if they are correlated and if they follow a gradual or episodic mode of evolution. To this end, we first produce the most complete time-calibrated phylogenetic tree for the order Scleractinia, including new sequences of never-before sampled species and genera. These novel sequences contribute to alleviate the current molecular under sampling of azooxanthellate species. Incorporating phylogenetic uncertainty, we obtained strong evidence in favor of a correlated and episodic model of evolution. This model led to the inference of an azooxanthellate and solitary most recent ancestor of scleractinians. Transition rates between the four different combinations of the two traits showed that while coloniality is gained and lost multiple times, symbiosis first appears around 282 Ma and is never lost. Also, coloniality seems to have appeared before symbiosis in azooxanthellate lineages. Thus, azooxanthellate corals, and especially colonial lineages, have been acting as a source of biodiversity for shallow zooxanthellate coral communities, highlighting the uniqueness of shallow and deep species and the need to preserve them.https://www.frontiersin.org/article/10.3389/fmars.2020.00461/fullScleractiniasymbiosiscolonialityzooxanthellaecorrelated evolutiondeep-sea |
| spellingShingle | Ana Navarro Campoy Ana Navarro Campoy Anna Maria Addamo Anna Maria Addamo Annie Machordom Andrew Meade Marcelo M. Rivadeneira Marcelo M. Rivadeneira Marcelo M. Rivadeneira Cristián E. Hernández Cristián E. Hernández Chris Venditti The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals Frontiers in Marine Science Scleractinia symbiosis coloniality zooxanthellae correlated evolution deep-sea |
| title | The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals |
| title_full | The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals |
| title_fullStr | The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals |
| title_full_unstemmed | The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals |
| title_short | The Origin and Correlated Evolution of Symbiosis and Coloniality in Scleractinian Corals |
| title_sort | origin and correlated evolution of symbiosis and coloniality in scleractinian corals |
| topic | Scleractinia symbiosis coloniality zooxanthellae correlated evolution deep-sea |
| url | https://www.frontiersin.org/article/10.3389/fmars.2020.00461/full |
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