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The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage

H Bradley Shaffer12*, Patrick Minx3*, Daniel E Warren4, Andrew M Shedlock56, Robert C Thomson7, Nicole Valenzuela8, John Abramyan9, Chris T Amemiya10, Daleen Badenhorst8, Kyle K Biggar11, Glen M Borchert1213, Christopher W Botka14, Rachel M Bowden12, Edward L Braun15, Anne M Bronikowski8, Benoit G Bruneau1617, Leslie T Buck18, Blanche Capel19, Todd A Castoe2021, Mike Czerwinski19, Kim D Delehaunty3, Scott V Edwards22, Catrina C Fronick3, Matthew K Fujita2123, Lucinda Fulton3, Tina A Graves3, Richard E Green24, Wilfried Haerty25, Ramkumar Hariharan26, Omar Hernandez27, LaDeana W Hillier3, Alisha K Holloway16, Daniel Janes8, Fredric J Janzen8, Cyriac Kandoth3, Lesheng Kong25, AP Jason de Koning20, Yang Li25, Robert Literman8, Suzanne E McGaugh28, Lindsey Mork19, Michelle O'Laughlin3, Ryan T Paitz12, David D Pollock20, Chris P Ponting25, Srihari Radhakrishnan298, Brian J Raney30, Joy M Richman9, John St John24, Tonia Schwartz298, Arun Sethuraman298, Phillip Q Spinks12, Kenneth B Storey11, Nay Thane3, Tomas Vinar31, Laura M Zimmerman12, Wesley C Warren3, Elaine R Mardis3 and Richard K Wilson3

Author affiliations

1 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA 90095-1606, USA

2 La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, University of California, Los Angeles, Los Angeles, CA 90095-1496, USA

3 The Genome Institute, Washington University School of Medicine, Campus Box 8501, 4444 Forest Park Avenue, St Louis, MO 63108, USA

4 Department of Biology, Saint Louis University, St Louis, MO 63103, USA

5 College of Charleston Biology Department and Grice Marine Laboratory, Charleston, SC 29424, USA

6 Medical University of South Carolina College of Graduate Studies and Center for Marine Biomedicine and Environmental Sciences, Charleston, SC 29412, USA

7 Department of Biology, University of Hawaii at Manoa, Honolulu, HI 96822, USA

8 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA

9 Faculty of Dentistry, Life Sciences Institute University of British Columbia, Vancouver BC, Canada

10 Benaroya Research Institute at Virginia Mason, Seattle, WA 98101 USA

11 Department of Biology and Institute of Biochemistry, Carleton University, Ottawa, ON, Canada K1S 5B6, Canada

12 School of Biological Sciences, Illinois State University, Normal, IL 61790, USA

13 Department of Biological Sciences, Life Sciences Building, University of South Alabama, Mobile, AL 36688-0002, USA

14 Research Computing, Harvard Medical School, Boston, MA 02115, USA

15 Department of Biology, University of Florida, Gainesville, FL 32611 USA

16 Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA

17 Cardiovascular Research Institute and Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94158, USA

18 Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5, Canada

19 Department of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA

20 Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA

21 Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA

22 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA

23 Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA

24 Baskin School of Engineering University of California, Santa Cruz Santa Cruz, CA 95064, USA

25 MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, Henry Wellcome Building of Gene Function, University of Oxford, Oxford, OX13PT, UK

26 Cancer Research Program, Rajiv Gandhi Centre for Biotechnology, Poojapura, Thycaud P.O, Thiruvananthapuram, Kerala 695014, India

27 FUDECI, Fundación para el Desarrollo de las Ciencias Físicas, Matemáticas y Naturales. Av, Universidad, Bolsa a San Francisco, Palacio de Las Academias, Caracas, Venezuela

28 Biology Department, Duke University, Durham, NC 27708, US

29 Bioinformatics and Computational Biology Laboratory, Iowa State University, Ames, IA 50011, USA

30 Center for Biomolecular Science and Engineering, School of Engineering, University of California Santa Cruz (UCSC), Santa Cruz, CA 95064, USA

31 Faculty of Mathematics, Physics and Informatics, Comenius University, Mlynska Dolina, Bratislava 84248, Slovakia

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Citation and License

Genome Biology 2013, 14:R28  doi:10.1186/gb-2013-14-3-r28

Published: 28 March 2013

Abstract

Background

We describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species' physiological capacities to withstand extreme anoxia and tissue freezing.

Results

Our phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented.

Conclusions

Our comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle's extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.

Keywords:
Amniote phylogeny; anoxia tolerance; chelonian; freeze tolerance; genomics; longevity; phylogenomics; physiology; turtle; evolutionary rates