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DNA capture reveals transoceanic gene flow in endangered river sharks

Chenhong Li, Shannon Corrigan, Lei Yang, Nicolas Straube, Mark Harris, Michael Hofreiter, William T. White, and Gavin J. P. Naylor
PNAS published ahead of print October 12, 2015 https://doi.org/10.1073/pnas.1508735112
Chenhong Li
aKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China;bHollings Marine Laboratory, College of Charleston, Charleston, SC 29412;
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Shannon Corrigan
bHollings Marine Laboratory, College of Charleston, Charleston, SC 29412;
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Lei Yang
bHollings Marine Laboratory, College of Charleston, Charleston, SC 29412;
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Nicolas Straube
bHollings Marine Laboratory, College of Charleston, Charleston, SC 29412;
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Mark Harris
cFlorida Fisheries Consultants Elasmobranch Studies, New Port Richey, FL 34655;
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Michael Hofreiter
dInstitute of Biochemistry and Biology, Faculty of Mathematics and Natural Sciences, University of Potsdam, 14476 Potsdam, Germany;
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William T. White
eWealth from Oceans Flagship, Commonwealth Scientific and Industrial Research Organisation Marine and Atmospheric Research, Hobart, TAS 7001, Australia
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Gavin J. P. Naylor
bHollings Marine Laboratory, College of Charleston, Charleston, SC 29412;
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  • ORCID record for Gavin J. P. Naylor
  • For correspondence: naylorg@cofc.edu
  1. Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved September 16, 2015 (received for review May 4, 2015)

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Significance

The river sharks of the genus Glyphis, widely feared as man-eaters throughout India, remain very poorly known to science. The group constitutes five described species, all of which are considered highly endangered and restricted to freshwater systems in Australasia and Southeast Asia. DNA sequence data derived from 19th-century dried museum material augmented with contemporary samples indicates that only three of the five currently described species are valid; that there is a genetically distinct, but as-yet-undescribed, species recorded in Bangladesh and Sarawak in Malaysian Borneo; and that these iconic and mysterious sharks are not restricted to freshwater at all but rather appear to be adapted to both marine and freshwater habitats.

Abstract

For over a hundred years, the “river sharks” of the genus Glyphis were only known from the type specimens of species that had been collected in the 19th century. They were widely considered extinct until populations of Glyphis-like sharks were rediscovered in remote regions of Borneo and Northern Australia at the end of the 20th century. However, the genetic affinities between the newly discovered Glyphis-like populations and the poorly preserved, original museum-type specimens have never been established. Here, we present the first (to our knowledge) fully resolved, complete phylogeny of Glyphis that includes both archival-type specimens and modern material. We used a sensitive DNA hybridization capture method to obtain complete mitochondrial genomes from all of our samples and show that three of the five described river shark species are probably conspecific and widely distributed in Southeast Asia. Furthermore we show that there has been recent gene flow between locations that are separated by large oceanic expanses. Our data strongly suggest marine dispersal in these species, overturning the widely held notion that river sharks are restricted to freshwater. It seems that species in the genus Glyphis are euryhaline with an ecology similar to the bull shark, in which adult individuals live in the ocean while the young grow up in river habitats with reduced predation pressure. Finally, we discovered a previously unidentified species within the genus Glyphis that is deeply divergent from all other lineages, underscoring the current lack of knowledge about the biodiversity and ecology of these mysterious sharks.

  • freshwater sharks
  • DNA
  • museum specimens

Footnotes

  • ↵1To whom correspondence should be addressed. Email: naylorg{at}cofc.edu.
  • Author contributions: C.L., S.C., and G.J.P.N. designed research; C.L., S.C., L.Y., N.S., M. Harris, and W.T.W. performed research; C.L., M. Hofreiter, and G.J.P.N. contributed new reagents/analytic tools; C.L., S.C., L.Y., M. Harris, W.T.W., and G.J.P.N. analyzed data; and C.L., S.C., M. Hofreiter, W.T.W., and G.J.P.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The mitochondrial sequences reported in this paper have been deposited in the GenBank database (accession nos. KT698039–KT698063). The nuclear dataset reported in this paper has been deposited in the TreeBASE database (study ID S18221).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1508735112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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River shark evolution
Chenhong Li, Shannon Corrigan, Lei Yang, Nicolas Straube, Mark Harris, Michael Hofreiter, William T. White, Gavin J. P. Naylor
Proceedings of the National Academy of Sciences Oct 2015, 201508735; DOI: 10.1073/pnas.1508735112

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River shark evolution
Chenhong Li, Shannon Corrigan, Lei Yang, Nicolas Straube, Mark Harris, Michael Hofreiter, William T. White, Gavin J. P. Naylor
Proceedings of the National Academy of Sciences Oct 2015, 201508735; DOI: 10.1073/pnas.1508735112
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