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The Tuatara Genome: Insights Into Vertebrate Evolution from the Sole Survivor of an Ancient Reptilian Order

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The Tuatara Genome: Insights Into Vertebrate Evolution from the Sole Survivor of an Ancient Reptilian Order bioRxiv preprint doi: https://doi.org/10.1101/867069; this version posted December 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The tuatara genome: insights into vertebrate evolution from the sole survivor of an ancient reptilian order 1 1 2,3 4,5 6 Neil J. Gemmell *​ Kim Rutherford ,​ Stefan Prost ,​ Marc Tollis ,​ David Winter ,​ J. ​ ​ ​ ​ ​ 7 8 9 8,10 11,12 Robert Macey ,​ David L. Adelson ,​ Alexander Suh ,​ Terry Bertozzi ,​ José H. Grau ,​ ​ ​ ​ ​ ​ 13 14 15 15 Chris Organ ,​ Paul P. Gardner ,​ Matthieu Muffato ,​ Mateus Patricio ,​ Konstantinos ​ ​ ​ ​ 15 15 15 16 17 Billis ,​ Fergal J Martin ,​ Paul Flicek ,​ Bent Petersen ,​ Lin Kang ,​ Pawel ​ ​ ​ ​ ​ 17-19, 20,21 4 22 Michalak ,​ Thomas R. Buckley ,​ Melissa Wilson ,​ Yuanyuan Cheng ​ , Hilary ​ ​ ​ ​ 23 24 25 25 Miller ,​ Ryan K. Schott ,​ Melissa Jordan ,​ Richard Newcomb ,​ José Ignacio ​ ​ ​ ​ 26 27 1 28 9 Arroyo ,​ Nicole Valenzuela ,​ Tim A. Hore ,​ Jaime Renart ,​ Valentina Peona ,​ Claire ​ ​ ​ ​ ​ 9,29 9,29 8 8 8 R. Peart ,​ Vera M. Warmuth ,​ Lu Zeng ,​ R. Daniel Kortschak ,​ Joy M. Raison ,​ ​ ​ ​ ​ ​ 27 27 30 30 Valeria Velásquez Zapata ,​ Zhiqiang Wu ,​ Didac Santesmasses ,​ Marco Mariotti ,​ ​ ​ ​ ​ 30 4 20,21 1 Roderic Guigó ,​ Shawn M. Rupp ,​ Victoria G. Twort ,​ Nicolas Dussex ,​ Helen ​ ​ ​ ​ 1 1 31 32 Taylor ,​ Hideaki Abe ,​ James M. Paterson ,​ Daniel G. Mulcahy ,​ Vanessa L. ​ ​ ​ ​ 32 7 7 33 Gonzalez ,​ Charles G. Barbieri ,​ Dustin P. DeMeo ,​ Stephan Pabinger ,​ Oliver ​ ​ ​ ​ 34 35 36 37 Ryder ,​ Scott V. Edwards ,​ Steven L. Salzberg ,​ Lindsay Mickelson ,​ Nicola ​ ​ ​ ​ 37 38 38 Nelson ,​ Clive Stone ,​ Ngatiwai Trust Board ​ ​ ​ 1. Allan Wilson Centre, Department of Anatomy, University of Otago, PO Box 56, Dunedin 9054, New Zealand 2. LOEWE-Center for Translational Biodiversity Genomics, Senckenberg Museum, 60325 Frankfurt, Germany 3. South African National Biodiversity Institute, National Zoological Garden, Pretoria, 0184, South Africa 4. School of Life Sciences, Arizona State University, 427 E Tyler Mall, Tempe, AZ 85281 USA 5. School of Informatics, Computing, and Cyber Systems, Northern Arizona University, 1295 S Knoles Drive, Flagstaff, AZ 86011 USA 6. School of Fundamental Sciences, Massey University, Private Bag 11 222, Palmerston North, 4442, New Zealand 7. Peralta Genomics Institute, Chancellor’s Office, Peralta Community College District, 333 East 8th Street, Oakland, CA 94606 8. School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia 9. Department of Ecology and Genetics - Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, Norbyvägen 18D, 75236 Uppsala, Sweden. 10. Evolutionary Biology Unit, South Australian Museum, Adelaide, SA 5000, Australia 11. Amedes Genetics, Amedes Medizinische Dienstleistungen GmbH, Jägerstr. 61, 10117 Berlin, Germany 12. Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin. Invalidenstraße 43, 10115. Berlin, Germany 13. Department of Earth Sciences, Montana State University, Bozeman, MT 59717 14. Department of Biochemistry, University of Otago, PO Box 56, Dunedin 9054, New Zealand 15. European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK 16. Section for Evolutionary Genomics, The GLOBE Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Øster Farimagsgade 5, 1353 København K, Denmark 17. Edward Via College of Osteopathic Medicine, Blacksburg, VA 24060, USA 18. Center for One Health Research, Virginia–Maryland College of Veterinary Medicine, Blacksburg, VA 24060, USA 19. Institute of Evolution, University of Haifa, Haifa, 3498838, Israel 20. Manaaki Whenua - Landcare Research, Private Bag 92170, Auckland, New Zealand 21. School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland, New Zealand ​ 22. School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia 23. Biomatters Ltd, Level 2, 18 Shortland Street, Auckland 1010 New Zealand 24. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC 20560, USA bioRxiv preprint doi: https://doi.org/10.1101/867069; this version posted December 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 2 25. The New Zealand Institute for Plant & Food Research, Private Bag 92169, Auckland, New Zealand 26. Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Avenida Libertador Bernardo O’Higgins 340, Santiago, Chile. 27. Iowa State University, Department of Ecology, Evolution, and Organismal Biology, 251 Bessey Hall, Ames IA, 5011 USA. 28. Instituto de Investigaciones Biomédicas CSIC-UAM, 28029-Madrid, Spain. 29. Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilian University of Munich, D-82152 Planegg-Martinsried, Germany 30. Centre for Genomic Regulation (CRG), The Barcelona Institute for Science and Technology, Barcelona, Catalonia, Spain, Universitat Pompeu Fabra (UPF), Barcelona, Catalonia, Spain 31. School of Biological Sciences, University of Canterbury, New Zealand 32. Global Genome Initiative, National Museum of Natural History, Smithsonian Institution, 1000 Constitution Ave., Washington, DC 20560, USA 33. AIT Austrian Institute of Technology, Center for Health and Bioresources, Molecular Diagnostics, Muthgasse 11, 1190 Vienna, Austria 34. San Diego Zoo Institute for Conservation Research, Escondido, CA 92027 USA 35. Department of Organismic and Evolutionary Biology and the Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 USA 36. Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21205 USA 37. School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington 6140, New Zealand 38. Ngatiwai Trust Board, 129 Port Road, PO Box 1332, Whangarei, New Zealand *Correspondence to: [email protected] The tuatara (Sphenodon punctatus), the only living member of the archaic reptilian ​ ​ order Rhynchocephalia (Sphenodontia) once widespread across Gondwana, is an iconic and enigmatic terrestrial vertebrate endemic to New Zealand. A key link to the now extinct stem reptiles from which dinosaurs, modern reptiles, birds and mammals evolved, the tuatara provides exclusive insights into the ancestral amniotes. The tuatara genome, at ~5 Gbp, is among the largest vertebrate genomes assembled. Analysis of this genome and comparisons to other vertebrates reinforces the uniqueness of the tuatara. Phylogenetic analyses indicate tuatara diverged from the snakes and lizards ~250 MYA. This lineage also shows moderate rates of molecular evolution, with instances of punctuated evolution. Genome sequence analysis identifies expansions of protein, non-protein-coding RNA families, and repeat elements, the latter of which show an extraordinary amalgam of reptilian and mammalian features. Sequencing of this genome provides a valuable resource for deep comparative analyses of tetrapods, as well as for tuatara biology and conservation. It also provides important insights into both the technical challenges and the cultural obligations associated with genome sequencing. The tuatara (Sphenodon punctatus) is an iconic and enigmatic terrestrial vertebrate, ​ 1 ​ unique to New Zealand .​ The only living member of the archaic reptilian order ​ Rhynchocephalia (Sphenodontia) which last shared a common ancestor with other reptiles some 250 million years ago (Figure 1), the tuatara represents an important link to the now extinct stem reptiles from which dinosaurs, modern reptiles, birds and 2 mammals evolved and is thus important for our understanding of amniote evolution .​ ​ bioRxiv preprint doi: https://doi.org/10.1101/867069; this version posted December 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 3 It is also a species of significance in other contexts. First, the tuatara is a taonga, or ​ ​ 1 special treasure, for Māori, who hold that tuatara are the guardians of special places .​ ​ Second, the tuatara is internationally recognised as a critically important species vulnerable to extinction due to habitat loss, predation, disease, global warming and 1 other factors .​ Third, the tuatara displays a variety of morphological and physiological ​ innovations that have puzzled scientists since the first description of the species in 1,3 1867 .​ These include a unique combination of features shared variously with lizards, ​ 1 turtles, and birds, which left its taxonomic position in doubt for many decades .​ That 4 ​ taxonomic conundrum has been largely addressed using molecular approaches ,​ but the ​ timing of the split of tuatara from the lineage that forms the modern squamata (lizards and snakes), the rate of evolution of tuatara, and the number of species of tuatara 1 remains contentious .​ Last, there are
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