Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

Author:

Green Richard E.1,Braun Edward L.2,Armstrong Joel13,Earl Dent13,Nguyen Ngan13,Hickey Glenn13,Vandewege Michael W.4,St. John John A.1,Capella-Gutiérrez Salvador56,Castoe Todd A.78,Kern Colin9,Fujita Matthew K.8,Opazo Juan C.10,Jurka Jerzy11,Kojima Kenji K.11,Caballero Juan12,Hubley Robert M.12,Smit Arian F.12,Platt Roy N.413,Lavoie Christine A.4,Ramakodi Meganathan P.413,Finger John W.14,Suh Alexander1516,Isberg Sally R.171819,Miles Lee18,Chong Amanda Y.18,Jaratlerdsiri Weerachai18,Gongora Jaime18,Moran Christopher18,Iriarte Andrés20,McCormack John21,Burgess Shane C.22,Edwards Scott V.23,Lyons Eric24,Williams Christina25,Breen Matthew25,Howard Jason T.26,Gresham Cathy R.13,Peterson Daniel G.1327,Schmitz Jürgen15,Pollock David D.7,Haussler David328,Triplett Eric W.29,Zhang Guojie3031,Irie Naoki32,Jarvis Erich D.26,Brochu Christopher A.33,Schmidt Carl J.34,McCarthy Fiona M.35,Faircloth Brant C.3637,Hoffmann Federico G.413,Glenn Travis C.14,Gabaldón Toni5638,Paten Benedict3,Ray David A.41339

Affiliation:

1. Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA.

2. Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.

3. Center for Biomolecular Science and Engineering, University of California, Santa Cruz, CA 95064, USA.

4. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA.

5. Bioinformatics and Genomics Programme, Centre for Genomic Regulation, 08003 Barcelona, Spain.

6. Universitat Pompeu Fabra, 08003 Barcelona, Spain.

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

8. Department of Biology, University of Texas, Arlington, TX 76019, USA.

9. Department of Computer and Information Sciences, University of Delaware, Newark, DE 19717, USA.

10. Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

11. Genetic Information Research Institute, Mountain View, CA 94043, USA.

12. Institute for Systems Biology, Seattle, WA 98109, USA.

13. Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.

14. Department of Environmental Health Science, University of Georgia, Athens, GA 30602, USA.

15. Institute of Experimental Pathology (ZMBE), University of Münster, D-48149 Münster, Germany.

16. Department of Evolutionary Biology (EBC), Uppsala University, SE-752 36 Uppsala, Sweden.

17. Porosus Pty. Ltd., Palmerston, NT 0831, Australia.

18. Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia.

19. Centre for Crocodile Research, Noonamah, NT 0837, Australia.

20. Departamento de Desarrollo Biotecnológico, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.

21. Moore Laboratory of Zoology, Occidental College, Los Angeles, CA 90041, USA.

22. College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ 85721, USA.

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

24. School of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA.

25. Department of Molecular Biomedical Sciences, North Carolina State University, Raleigh, NC 27607, USA.

26. Howard Hughes Medical Institute, Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA.

27. Department of Plant and Soil Sciences, Mississippi State University, Mississippi State, MS 39762, USA.

28. Howard Hughes Medical Institute, Bethesda, MD 20814, USA.

29. Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611, USA.

30. China National GeneBank, BGI-Shenzhen, Shenzhen, China.

31. Center for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

32. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan.

33. Department of Earth and Environmental Sciences, University of Iowa, Iowa City, IA 52242, USA.

34. Department of Animal and Food Sciences, University of Delaware, Newark, DE 19717, USA.

35. School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ 85721, USA.

36. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90019, USA.

37. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.

38. Institució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain.

39. Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA.

Abstract

To provide context for the diversification of archosaurs—the group that includes crocodilians, dinosaurs, and birds—we generated draft genomes of three crocodilians: Alligator mississippiensis (the American alligator), Crocodylus porosus (the saltwater crocodile), and Gavialis gangeticus (the Indian gharial). We observed an exceptionally slow rate of genome evolution within crocodilians at all levels, including nucleotide substitutions, indels, transposable element content and movement, gene family evolution, and chromosomal synteny. When placed within the context of related taxa including birds and turtles, this suggests that the common ancestor of all of these taxa also exhibited slow genome evolution and that the comparatively rapid evolution is derived in birds. The data also provided the opportunity to analyze heterozygosity in crocodilians, which indicates a likely reduction in population size for all three taxa through the Pleistocene. Finally, these data combined with newly published bird genomes allowed us to reconstruct the partial genome of the common ancestor of archosaurs, thereby providing a tool to investigate the genetic starting material of crocodilians, birds, and dinosaurs.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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