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Research Article

Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil)

Webb Miller, Vanessa M. Hayes, Aakrosh Ratan, Desiree C. Petersen, Nicola E. Wittekindt, Jason Miller, Brian Walenz, James Knight, Ji Qi, Fangqing Zhao, Qingyu Wang, Oscar C. Bedoya-Reina, Neerja Katiyar, Lynn P. Tomsho, Lindsay McClellan Kasson, Rae-Anne Hardie, Paula Woodbridge, Elizabeth A. Tindall, Mads Frost Bertelsen, Dale Dixon, Stephen Pyecroft, Kristofer M. Helgen, Arthur M. Lesk, Thomas H. Pringle, Nick Patterson, Yu Zhang, Alexandre Kreiss, Gregory M. Woods, Menna E. Jones, and Stephan C. Schuster
  1. aPennsylvania State University, Center for Comparative Genomics and Bioinformatics, University Park, PA 16802;
  2. bChildren's Cancer Institute Australia and University of New South Wales, Lowy Cancer Research Centre, Randwick, NSW 2031, Australia;
  3. cThe J. Craig Venter Institute, Rockville, MD 20850;
  4. d454 Life Sciences, Branford, CT 06405;
  5. eCenter for Zoo and Wild Animal Health, Copenhagen Zoo, 2000 Frederiksberg, Denmark;
  6. fMuseum and Art Gallery of the Northern Territory, Darwin 0801, Australia;
  7. gDepartment of Primary Industries and Water, Mt. Pleasant Animal Health Laboratories, Kings Meadows, Tasmania 7249, Australia;
  8. hNational Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012;
  9. iThe Sperling Foundation, Eugene, OR 97405;
  10. jBroad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge Center, Cambridge, MA 02142;
  11. kUniversity of Tasmania, Hobart, TAS 7001, Australia; and
  12. lImmunology, Menzies Research Institute, Hobart, Tasmania 7000, Australia

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PNAS first published June 27, 2011; https://doi.org/10.1073/pnas.1102838108
Webb Miller
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Vanessa M. Hayes
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  • For correspondence: vhayes@jcvi.org scs@bx.psu.edu
Aakrosh Ratan
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Desiree C. Petersen
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Nicola E. Wittekindt
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Jason Miller
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Brian Walenz
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James Knight
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Ji Qi
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Fangqing Zhao
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Qingyu Wang
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Oscar C. Bedoya-Reina
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Neerja Katiyar
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Lynn P. Tomsho
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Lindsay McClellan Kasson
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Rae-Anne Hardie
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Paula Woodbridge
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Elizabeth A. Tindall
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Mads Frost Bertelsen
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Dale Dixon
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Stephen Pyecroft
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Kristofer M. Helgen
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Arthur M. Lesk
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Thomas H. Pringle
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Nick Patterson
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Yu Zhang
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Alexandre Kreiss
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Gregory M. Woods
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Menna E. Jones
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Stephan C. Schuster
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  • For correspondence: vhayes@jcvi.org scs@bx.psu.edu
  1. Edited* by Luis Herrera Estrella, Center for Research and Advanced Studies, Irapuato, Mexico, and approved May 23, 2011 (received for review February 24, 2011)

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Abstract

The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction because of a contagious cancer known as Devil Facial Tumor Disease. The inability to mount an immune response and to reject these tumors might be caused by a lack of genetic diversity within a dwindling population. Here we report a whole-genome analysis of two animals originating from extreme northwest and southeast Tasmania, the maximal geographic spread, together with the genome from a tumor taken from one of them. A 3.3-Gb de novo assembly of the sequence data from two complementary next-generation sequencing platforms was used to identify 1 million polymorphic genomic positions, roughly one-quarter of the number observed between two genetically distant human genomes. Analysis of 14 complete mitochondrial genomes from current and museum specimens, as well as mitochondrial and nuclear SNP markers in 175 animals, suggests that the observed low genetic diversity in today's population preceded the Devil Facial Tumor Disease disease outbreak by at least 100 y. Using a genetically characterized breeding stock based on the genome sequence will enable preservation of the extant genetic diversity in future Tasmanian devil populations.

  • wildlife conservation
  • ancient DNA
  • population genetics
  • semiconductor sequencing
  • selective breeding

Footnotes

  • ↵1W.M., V.M.H., and S.C.S. contributed equally to this work.

  • 2To whom correspondence may be addressed. E-mail: vhayes{at}jcvi.org or scs{at}bx.psu.edu.
  • Author contributions: W.M., V.M.H., and S.C.S. designed research; M.F.B., D.D., S.P., K.M.H., A.K., G.M.W., and M.E.J. directed field studies and provided samples; W.M., V.M.H., A.R., D.C.P., N.E.W., J.M., B.W., J.K., J.Q., F.Z., Q.W., O.C.B.-R., N.K., L.P.T., L.M.K., R.-A.H., P.W., E.A.T., M.F.B., D.D., S.P., K.M.H., A.M.L., T.H.P., N.P., Y.Z., A.K., G.M.W., M.E.J., and S.C.S. analyzed data; and S.C.S. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. AFEY00000000).

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1102838108/-/DCSupplemental.

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Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil)
Webb Miller, Vanessa M. Hayes, Aakrosh Ratan, Desiree C. Petersen, Nicola E. Wittekindt, Jason Miller, Brian Walenz, James Knight, Ji Qi, Fangqing Zhao, Qingyu Wang, Oscar C. Bedoya-Reina, Neerja Katiyar, Lynn P. Tomsho, Lindsay McClellan Kasson, Rae-Anne Hardie, Paula Woodbridge, Elizabeth A. Tindall, Mads Frost Bertelsen, Dale Dixon, Stephen Pyecroft, Kristofer M. Helgen, Arthur M. Lesk, Thomas H. Pringle, Nick Patterson, Yu Zhang, Alexandre Kreiss, Gregory M. Woods, Menna E. Jones, Stephan C. Schuster
Proceedings of the National Academy of Sciences Jun 2011, 201102838; DOI: 10.1073/pnas.1102838108

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Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil)
Webb Miller, Vanessa M. Hayes, Aakrosh Ratan, Desiree C. Petersen, Nicola E. Wittekindt, Jason Miller, Brian Walenz, James Knight, Ji Qi, Fangqing Zhao, Qingyu Wang, Oscar C. Bedoya-Reina, Neerja Katiyar, Lynn P. Tomsho, Lindsay McClellan Kasson, Rae-Anne Hardie, Paula Woodbridge, Elizabeth A. Tindall, Mads Frost Bertelsen, Dale Dixon, Stephen Pyecroft, Kristofer M. Helgen, Arthur M. Lesk, Thomas H. Pringle, Nick Patterson, Yu Zhang, Alexandre Kreiss, Gregory M. Woods, Menna E. Jones, Stephan C. Schuster
Proceedings of the National Academy of Sciences Jun 2011, 201102838; DOI: 10.1073/pnas.1102838108
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