Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

Richard E Green; Edward L Braun; Joel Armstrong; Dent Earl; Ngan Nguyen; Glenn Hickey; Michael W Vandewege; John A St John; Salvador Capella-Gutiérrez; Todd A Castoe; Colin Kern; Matthew K Fujita; Juan C Opazo; Jerzy Jurka; Kenji K Kojima; Juan Caballero; Robert M Hubley; Arian F Smit; Roy N Platt; Christine A Lavoie; Meganathan P Ramakodi; John W Finger Jr; Alexander Suh; Sally R Isberg; Lee Miles; Amanda Y Chong; Weerachai Jaratlerdsiri; Jaime Gongora; Christopher Moran; Andrés Iriarte; John McCormack; Shane C Burgess; Scott V Edwards; Eric Lyons; Christina Williams; Matthew Breen; Jason T Howard; Cathy R Gresham; Daniel G Peterson; Jürgen Schmitz; David D Pollock; David Haussler; Eric W Triplett; Guojie Zhang; Naoki Irie; Erich D Jarvis; Christopher A Brochu; Carl J Schmidt; Fiona M McCarthy; Brant C Faircloth; Federico G Hoffmann; Travis C Glenn; Toni Gabaldón; Benedict Paten; David A Ray

doi:10.1126/science.1254449

Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

Science. 2014 Dec 12;346(6215):1254449. doi: 10.1126/science.1254449. Epub 2014 Dec 11.

Authors

Richard E Green¹, Edward L Braun², Joel Armstrong³, Dent Earl³, Ngan Nguyen³, Glenn Hickey³, Michael W Vandewege⁴, John A St John⁵, Salvador Capella-Gutiérrez⁶, Todd A Castoe⁷, Colin Kern⁸, Matthew K Fujita⁹, Juan C Opazo¹⁰, Jerzy Jurka¹¹, Kenji K Kojima¹¹, Juan Caballero¹², Robert M Hubley¹², Arian F Smit¹², Roy N Platt¹³, Christine A Lavoie⁴, Meganathan P Ramakodi¹³, John W Finger Jr¹⁴, Alexander Suh¹⁵, Sally R Isberg¹⁶, Lee Miles¹⁷, Amanda Y Chong¹⁷, Weerachai Jaratlerdsiri¹⁷, Jaime Gongora¹⁷, Christopher Moran¹⁷, Andrés Iriarte¹⁸, John McCormack¹⁹, Shane C Burgess²⁰, Scott V Edwards²¹, Eric Lyons²², Christina Williams²³, Matthew Breen²³, Jason T Howard²⁴, Cathy R Gresham²⁵, Daniel G Peterson²⁶, Jürgen Schmitz²⁷, David D Pollock²⁸, David Haussler²⁹, Eric W Triplett³⁰, Guojie Zhang³¹, Naoki Irie³², Erich D Jarvis²⁴, Christopher A Brochu³³, Carl J Schmidt³⁴, Fiona M McCarthy³⁵, Brant C Faircloth³⁶, Federico G Hoffmann¹³, Travis C Glenn¹⁴, Toni Gabaldón³⁷, Benedict Paten³⁸, David A Ray³⁹

Affiliations

¹ Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA. ed@soe.ucsc.edu david.a.ray@ttu.edu.
² Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.
³ Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA. 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 Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA.
⁶ Bioinformatics and Genomics Programme, Centre for Genomic Regulation, 08003 Barcelona, Spain. Universitat Pompeu Fabra, 08003 Barcelona, Spain.
⁷ Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA. Department of Biology, University of Texas, Arlington, TX 76019, USA.
⁸ Department of Computer and Information Sciences, University of Delaware, Newark, DE 19717, USA.
⁹ Department of Biology, University of Texas, Arlington, TX 76019, 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 Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA. 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. Department of Evolutionary Biology (EBC), Uppsala University, SE-752 36 Uppsala, Sweden.
¹⁶ Porosus Pty. Ltd., Palmerston, NT 0831, Australia. Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia. Centre for Crocodile Research, Noonamah, NT 0837, Australia.
¹⁷ Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia.
¹⁸ Departamento de Desarrollo Biotecnológico, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
¹⁹ Moore Laboratory of Zoology, Occidental College, Los Angeles, CA 90041, USA.
²⁰ College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ 85721, USA.
²¹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
²² School of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA.
²³ Department of Molecular Biomedical Sciences, North Carolina State University, Raleigh, NC 27607, USA.
²⁴ Howard Hughes Medical Institute, Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA.
²⁵ Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
²⁶ Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA. Department of Plant and Soil Sciences, Mississippi State University, Mississippi State, MS 39762, USA.
²⁷ Institute of Experimental Pathology (ZMBE), University of Münster, D-48149 Münster, Germany.
²⁸ Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA.
²⁹ Center for Biomolecular Science and Engineering, University of California, Santa Cruz, CA 95064, USA. Howard Hughes Medical Institute, Bethesda, MD 20814, USA.
³⁰ Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611, USA.
³¹ China National GeneBank, BGI-Shenzhen, Shenzhen, China. 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. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
³⁷ Bioinformatics and Genomics Programme, Centre for Genomic Regulation, 08003 Barcelona, Spain. Universitat Pompeu Fabra, 08003 Barcelona, Spain. Institució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain.
³⁸ Center for Biomolecular Science and Engineering, University of California, Santa Cruz, CA 95064, USA.
³⁹ Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA. Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA. Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA. ed@soe.ucsc.edu david.a.ray@ttu.edu.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Alligators and Crocodiles / classification
Alligators and Crocodiles / genetics*
Animals
Biological Evolution
Birds / classification
Birds / genetics*
Conserved Sequence
DNA Transposable Elements
Dinosaurs / classification
Dinosaurs / genetics*
Evolution, Molecular*
Genetic Variation
Genome*
Molecular Sequence Annotation
Molecular Sequence Data
Phylogeny
Reptiles / classification
Reptiles / genetics
Sequence Alignment
Sequence Analysis, DNA
Transcriptome

Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

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