Skip to main content

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home
  • Log in
  • My Cart

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
Research Article

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

Benjamin C. C. Hume, Christian R. Voolstra, Chatchanit Arif, Cecilia D’Angelo, John A. Burt, Gal Eyal, Yossi Loya, and Jörg Wiedenmann
  1. aCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
  2. 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;
  3. cInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
  4. dMarine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi 129188, United Arab Emirates;
  5. eDepartment of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
  6. fThe Interuniversity Institute for Marine Sciences in Eilat, Eilat 8810369, Israel

See allHide authors and affiliations

PNAS April 19, 2016 113 (16) 4416-4421; first published April 4, 2016; https://doi.org/10.1073/pnas.1601910113
Benjamin C. C. Hume
aCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Christian R. Voolstra
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;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Chatchanit Arif
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;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Cecilia D’Angelo
aCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
cInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
John A. Burt
dMarine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi 129188, United Arab Emirates;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gal Eyal
eDepartment of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
fThe Interuniversity Institute for Marine Sciences in Eilat, Eilat 8810369, Israel
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yossi Loya
eDepartment of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jörg Wiedenmann
aCoral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
cInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: joerg.wiedenmann@noc.soton.ac.uk
  1. Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved March 3, 2016 (received for review February 4, 2016)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

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.

  • Persian/Arabian Gulf
  • adaptation
  • coral
  • Symbiodinium
  • climate change

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.

View Full Text
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Ancestral diversity linked to climate adaptation
Benjamin C. C. Hume, Christian R. Voolstra, Chatchanit Arif, Cecilia D’Angelo, John A. Burt, Gal Eyal, Yossi Loya, Jörg Wiedenmann
Proceedings of the National Academy of Sciences Apr 2016, 113 (16) 4416-4421; DOI: 10.1073/pnas.1601910113

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Ancestral diversity linked to climate adaptation
Benjamin C. C. Hume, Christian R. Voolstra, Chatchanit Arif, Cecilia D’Angelo, John A. Burt, Gal Eyal, Yossi Loya, Jörg Wiedenmann
Proceedings of the National Academy of Sciences Apr 2016, 113 (16) 4416-4421; DOI: 10.1073/pnas.1601910113
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley

Article Classifications

  • Biological Sciences
  • Evolution
Proceedings of the National Academy of Sciences: 113 (16)
Table of Contents

Submit

Sign up for Article Alerts

Jump to section

  • Article
    • Abstract
    • Results and Discussion
    • Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Water from a faucet fills a glass.
News Feature: How “forever chemicals” might impair the immune system
Researchers are exploring whether these ubiquitous fluorinated molecules might worsen infections or hamper vaccine effectiveness.
Image credit: Shutterstock/Dmitry Naumov.
Reflection of clouds in the still waters of Mono Lake in California.
Inner Workings: Making headway with the mysteries of life’s origins
Recent experiments and simulations are starting to answer some fundamental questions about how life came to be.
Image credit: Shutterstock/Radoslaw Lecyk.
Cave in coastal Kenya with tree growing in the middle.
Journal Club: Small, sharp blades mark shift from Middle to Later Stone Age in coastal Kenya
Archaeologists have long tried to define the transition between the two time periods.
Image credit: Ceri Shipton.
Mouse fibroblast cells. Electron bifurcation reactions keep mammalian cells alive.
Exploring electron bifurcation
Jonathon Yuly, David Beratan, and Peng Zhang investigate how electron bifurcation reactions work.
Listen
Past PodcastsSubscribe
Panda bear hanging in a tree
How horse manure helps giant pandas tolerate cold
A study finds that giant pandas roll in horse manure to increase their cold tolerance.
Image credit: Fuwen Wei.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Subscribers
  • Librarians
  • Press
  • Cozzarelli Prize
  • Site Map
  • PNAS Updates
  • FAQs
  • Accessibility Statement
  • Rights & Permissions
  • About
  • Contact

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490