Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Handle URI:
http://hdl.handle.net/10754/621450
Title:
Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change
Authors:
Hume, Benjamin C. C.; Voolstra, Christian R. ( 0000-0003-4555-3795 ) ; Arif, Chatchanit ( 0000-0001-5640-9970 ) ; D’Angelo, Cecilia; Burt, John A.; Eyal, Gal; Loya, Yossi; Wiedenmann, Jörg
Abstract:
Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6, 000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5, 000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Environmental Science and Engineering Program; Red Sea Research Center (RSRC)
Citation:
Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, et al. (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci USA 113: 4416–4421. Available: http://dx.doi.org/10.1073/pnas.1601910113.
Publisher:
Proceedings of the National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences
Issue Date:
5-Apr-2016
DOI:
10.1073/pnas.1601910113
Type:
Article
ISSN:
0027-8424; 1091-6490
Sponsors:
We appreciate the help of Cornelia Roder, Sergey Dobretsov, Julia Schnetzer, Todd LaJeunesse, and Drew Wham with sample collection. A. Al-Hemeri (UAE Federal Environment Agency), A. Al-Cibahy (Environment Agency of Abu Dhabi), and the Oman Ministry of Environment & Climate Affairs kindly provided Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) export permits (no. 09FEA555) and collection permits. We acknowledge Tropical Marine Centre (London) and Tropic Marin (Wartenberg) for sponsoring the Coral Reef Laboratory at the University of Southampton. We thank the NYU Abu Dhabi Institute for supporting the 2012/2013 field workshops during which samples for this study were collected and the Interuniversity Institute for Marine Sciences in Eilat for field work support. The study was funded by Natural Environment Research Council Grant NE/K00641X/1 (to J.W.), the European Research Council under the European Union's Seventh Framework Programme Grant FP7/2007-2013/ERC Grant Agreement 311179 (to J.W.), the King Abdullah University of Science and Technology (C.R.V.), and Israel Science Foundation Grant 341/12, United States Agency for International Development/Middle East Regional Co-operation (USAID/MERC) No. M32-037 (to Y.L.).
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Environmental Science and Engineering Program; Biological and Environmental Sciences and Engineering (BESE) Division; Reef Genomics, part of the Global Ocean Genome Project

Full metadata record

DC FieldValue Language
dc.contributor.authorHume, Benjamin C. C.en
dc.contributor.authorVoolstra, Christian R.en
dc.contributor.authorArif, Chatchaniten
dc.contributor.authorD’Angelo, Ceciliaen
dc.contributor.authorBurt, John A.en
dc.contributor.authorEyal, Galen
dc.contributor.authorLoya, Yossien
dc.contributor.authorWiedenmann, Jörgen
dc.date.accessioned2016-11-03T08:29:37Z-
dc.date.available2016-11-03T08:29:37Z-
dc.date.issued2016-04-05en
dc.identifier.citationHume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, et al. (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci USA 113: 4416–4421. Available: http://dx.doi.org/10.1073/pnas.1601910113.en
dc.identifier.issn0027-8424en
dc.identifier.issn1091-6490en
dc.identifier.doi10.1073/pnas.1601910113en
dc.identifier.urihttp://hdl.handle.net/10754/621450-
dc.description.abstractCoral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6, 000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5, 000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.en
dc.description.sponsorshipWe appreciate the help of Cornelia Roder, Sergey Dobretsov, Julia Schnetzer, Todd LaJeunesse, and Drew Wham with sample collection. A. Al-Hemeri (UAE Federal Environment Agency), A. Al-Cibahy (Environment Agency of Abu Dhabi), and the Oman Ministry of Environment & Climate Affairs kindly provided Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) export permits (no. 09FEA555) and collection permits. We acknowledge Tropical Marine Centre (London) and Tropic Marin (Wartenberg) for sponsoring the Coral Reef Laboratory at the University of Southampton. We thank the NYU Abu Dhabi Institute for supporting the 2012/2013 field workshops during which samples for this study were collected and the Interuniversity Institute for Marine Sciences in Eilat for field work support. The study was funded by Natural Environment Research Council Grant NE/K00641X/1 (to J.W.), the European Research Council under the European Union's Seventh Framework Programme Grant FP7/2007-2013/ERC Grant Agreement 311179 (to J.W.), the King Abdullah University of Science and Technology (C.R.V.), and Israel Science Foundation Grant 341/12, United States Agency for International Development/Middle East Regional Co-operation (USAID/MERC) No. M32-037 (to Y.L.).en
dc.publisherProceedings of the National Academy of Sciencesen
dc.subjectAdaptationen
dc.subjectClimate changeen
dc.subjectCoralen
dc.subjectPersian/Arabian Gulfen
dc.subjectSymbiodiniumen
dc.titleAncestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate changeen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentEnvironmental Science and Engineering Programen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalProceedings of the National Academy of Sciencesen
dc.contributor.institutionCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton, United Kingdomen
dc.contributor.institutionInstitute for Life Sciences, University of Southampton, Southampton, United Kingdomen
dc.contributor.institutionMarine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emiratesen
dc.contributor.institutionDepartment of Zoology, Tel Aviv University, Tel Aviv, Israelen
dc.contributor.institutionInteruniversity Institute for Marine Sciences in Eilat, Eilat, Israelen
kaust.authorVoolstra, Christian R.en
kaust.authorArif, Chatchaniten
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