Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change
- aCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
- bRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia;
- cInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
- dMarine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi 129188, United Arab Emirates;
- eDepartment of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
- fThe Interuniversity Institute for Marine Sciences in Eilat, Eilat 8810369, Israel
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Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved March 3, 2016 (received for review February 4, 2016)

Significance
Reef corals in the Persian/Arabian Gulf (PAG) withstand exceptionally high salinity and regular summer temperatures of ∼35 °C that kill conspecifics elsewhere. These thermotolerant communities established themselves within only ∼6,000 y under the pressure of rapid climate change and can therefore inform how other coral reefs may respond to global warming. One key to the thermotolerance of PAG corals is their symbiosis with Symbiodinium thermophilum. Phylogeographic evidence indicates that this symbiont represents a stress-tolerant subpopulation of an ancestral taxonomic group with surprising genetic diversity that exists at barely detectable levels outside the PAG. Our results highlight the critical importance of present-day biodiversity for future adaptation to climate change for coral reefs and ecosystems in general.
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.
Footnotes
- ↵1To whom correspondence should be addressed. Email: joerg.wiedenmann{at}noc.soton.ac.uk.
Author contributions: B.C.C.H., C.R.V., and J.W. designed research; B.C.C.H., C.R.V., and C.A. performed research; B.C.C.H., C.R.V., J.A.B., G.E., Y.L., and J.W. performed field work; B.C.C.H., C.R.V., C.A., C.D., and J.W. analyzed data; and B.C.C.H., C.D., and J.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KR996268–KR996464 and KT156647–KT156665).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1601910113/-/DCSupplemental.
Freely available online through the PNAS open access option.
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