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

H. Bradley Shaffer, University of California, Los Angeles
Patrick Minx, Washington University School of Medicine in St. Louis
Daniel E. Warren, Saint Louis University
Andrew M. Shedlock, College of Charleston
Robert C. Thompson, University of Hawaiʻi at Mānoa
Nicole M. Valenzuela, Iowa State University
John Abramyan, University of British Columbia
Chris T. Amemiya, Benaroya Research Institute at Virginia Mason
Daleen Badenhorst, Iowa State University
Kyle K. Biggar, Carleton University
Glen M. Borchert, Illinois State University
Christopher W. Botka, Harvard Medical School
Rachel M. Bowden, Illinois State University
Edward L. Braun, University of Florida
Anne M. Bronikowski, Iowa State University
Benoit G. Bruneau, University of California, San Francisco
Leslie T. Buck, University of Toronto
Blanche Capel, Duke University
Todd A. Castoe, University of Colorado
Mike Czerwinski, Duke University
Kim D. Delehaunty, Washington University School of Medicine in St. Louis
Scott V. Edwards, Harvard University
Catrina C. Fronick, Washington University School of Medicine in St. Louis
Matthew K. Fujita, University of Texas at Arlington
Lucinda Fulton, Washington University School of Medicine in St. Louis
Tina A. Graves, Washington University School of Medicine in St. Louis
Richard E. Green, University of California, Santa Cruz
Wilfried Haerty, University of Oxford
Ramkumar Hariharan, Rajiv Gandhi Centre for Biotechnology
Omar Hernandez, Fundación Para el Desarrollo de las Ciencias Físicas, Matemáticas y Naturale
LaDeana W. Hillier, Washington University School of Medicine in St. Louis
Alisha K. Holloway, Gladstone Institute of Cardiovascular Disease
Daniel Janes, Iowa State University
Fredric J. Janzen, Iowa State University
Cyriac Kandoth, Washington University School of Medicine in St. Louis
Lesheng Kong, University of Oxford
AP Jason de Koning, University of Colorado
Yang Li, University of Oxford
Robert A. Literman, Iowa State University
Suzanne E. McGaugh, Duke University
Lindsey Mork, Duke University
Michelle O'Laughlin, Washington University School of Medicine in St. Louis
Ryan T. Paitz, Illinois State University
David D. Pollock, University of Colorado
Chris P. Ponting, University of Oxford
Srihari Radhakrishnan, Iowa State University
Brian J. Raney, University of California, Santa Cruz
Joy M. Richman, University of British Columbia
John St. John, University of California, Santa Cruz
Tonia Sue Schwartz, Iowa State University
Arun Sethuraman, Iowa State University
Phillip Q. Spinks, University of California, Los Angeles
Kenneth B. Storey, Carleton University
Nay Thane, Washington University School of Medicine in St. Louis
Tomas Vinar, Comenius University
Laura M. Zimmerman, Illinois State University
Wesley C. Warren, Washington University School of Medicine in St. Louis
Elaine R. Mardis, Washington University School of Medicine in St. Louis
Richard K. Wilson, Washington University School of Medicine in St. Louis

This article is from Genome Biology 14 (2013): R28, doi:10.1186/gb-2013-14-3-r28. Posted with permission.

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.