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Green Pages 1..9 ary change rather than intrinsic differences RESEARCH ARTICLE SUMMARY in base-repair machinery. We hypothesize that this single cause may be a consistently AVIAN GENOMICS longer generation time over the evolution- ary history of Crocodylia. Low heterozygosity was observed in each Three crocodilian genomes reveal genome, consistent with previous analyses, including the Chinese alligator. Pairwise ancestral patterns of evolution sequential Markov chain analysis of re- gional heterozygosity indicates that during glacial cycles of the Pleistocene, each spe- among archosaurs cies suffered reductions in effective popu- Richard E. Green,* Edward L. Braun, Joel Armstrong, Dent Earl, Ngan Nguyen, lation size. The reduction was especially Glenn Hickey, Michael W. Vandewege, John A. St. John, Salvador Capella-Gutiérrez, strong for the American alligator, whose Todd A. Castoe, Colin Kern, Matthew K. Fujita, Juan C. Opazo, Jerzy Jurka, current range extends farthest into regions Kenji K. Kojima, Juan Caballero, Robert M. Hubley, Arian F. Smit, Roy N. Platt, of temperate climates. Christine A. Lavoie, Meganathan P. Ramakodi, John W. Finger Jr., Alexander Suh, Sally R. Isberg, Lee Miles, Amanda Y. Chong, Weerachai Jaratlerdsiri, Jaime Gongora, CONCLUSION: We used crocodilian, avian, Christopher Moran, Andrés Iriarte, John McCormack, Shane C. Burgess, Scott V. Edwards, and outgroup genomes to reconstruct 584 Eric Lyons, Christina Williams, Matthew Breen, Jason T. Howard, Cathy R. Gresham, megabases of the archosaurian common Daniel G. Peterson, Jürgen Schmitz, David D. Pollock, David Haussler, Eric W. Triplett, ancestor genome and the genomes of key Guojie Zhang, Naoki Irie, Erich D. Jarvis, Christopher A. Brochu, Carl J. Schmidt, ancestral nodes. The estimated accuracy of Fiona M. McCarthy, Brant C. Faircloth, Federico G. Hoffmann, Travis C. Glenn, the archosaurian genome reconstruction Toni Gabaldón, Benedict Paten, David A. Ray* is 91% and is higher for conserved regions such as genes. The reconstructed genome INTRODUCTION: Crocodilians and birds reptile genome sequences, we generated can be improved by adding more crocodil- are the two extant clades of archosaurs, a phylogenies that confirm the sister rela- ian and avian genome assemblies and may on December 15, 2014 group that includes the extinct dinosaurs tionship between crocodiles and gharials, provide a unique window to the genomes and pterosaurs. Fossils suggest that living the relationship with birds as members of of extinct organisms such as dinosaurs crocodilians (alligators, extant Archosauria, and the outgroup sta- and pterosaurs. ■ ON OUR WEB SITE crocodiles, and ghari- tus of turtles relative to als) have a most recent birds and crocodilians. Read the full article Coelacanth at http://dx.doi common ancestor 80 to We also estimated .org/10.1126/ 100 million years ago. evolutionary rates along Platypus science.1254449 Extant crocodilians branches of the tetra- Opossum are notable for their pod p h y l o g e n y u s i n g Armadillo www.sciencemag.org distinct morphology, limited intraspecific two approaches: ultra- Elephant variation, and slow karyotype evolution. c o n s e r v e d e l e m e n t – Dog Despite their unique biology and phyloge- a nchored sequences and Mouse netic position, little is known about genome fourfold degenerate sites evolution within crocodilians. w i t h i n s t r i n g e n t l y f il- Human tered orthologous gene Python RATIONALE: Genome sequences for the alignments. Both analy- Lizard American alligator, saltwater crocodile, and ses indicate that the Green sea turtle Downloaded from Fast Indian gharial—representatives of all three rates of base substitution Chinese softshell turtle extant crocodilian families—were obtained a l o n g t h e c r o c o d i l i a n Alligator to facilitate better understanding of the and turtle lineages are te a r unique biology of this group and provide extremely low. Support- y r a Gharial a context for studying avian genome evolu- ing observations were n o tion. Sequence data from these three croco- m a d e f o r t r a n s pos- ti u l ? Crocodile o dilians and birds also allow reconstruction able e l e m e n t c o n t e n t v Ostrich E of the ancestral archosaurian genome. a n d f o r g e n e f a m i l y Chicken evolution. A n a l y s i s of Slow Penguin RESULTS: We sequenced shotgun genomic w h o l e - g e n o m e a l i gn- ? libraries from each species and used a va- ments across a panel of Pigeon riety of assembly strategies to obtain draft reptiles and mammals Zebra fnch genomes for these three crocodilians. The showed that the rate of assembled scaffold N50 was highest for the accumulation of micro- Evolutionary rates of tetrapods inferred from DNA sequenc- alligator (508 kilobases). Using a panel of insertions and microde- es anchored by ultraconser ved elements. Evolutionary rates letions is proportionally among reptiles vary, with especially low rates among extant A complete list of affiliations is available in the full article online. lower in crocodilians, crocodilians but high rates among squamates. We have recon- *Corresponding author. E-mail: [email protected] (R.E.G.); consistent with a single structed the genomes of the common ancestor of birds and of all [email protected] (D.A.R.) Cite this article as R. E. Green et al., Science 346, 1254449 underlying cause of a re- archosaurs (shown in gray silhouette, although the morphology (2014). DOI: 10.1126/science.1254449 duced rate of evolution- of these species is uncertain). SCIENCE sciencemag.org 12 DECEMBER 2014 • VOL 346 ISSUE 6215 1335 Published by AAAS RESEARCH ARTICLE pair libraries from each species: alligator, croco- dile,andgharial.Theassemblystrategyforeach taxon differed because of varying legacy data and developments in library preparation meth- Three crocodilian genomes reveal odsduringthecourseoftheproject(17). Genome scaffolding of the alligator (and, to a lesser ex- ancestral patterns of evolution tent, the crocodile) was aided by the availability among archosaurs 1Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA. 2Department of 1 2 1,3 1,3 Biology and Genetics Institute, University of Florida, Richard E. Green, * Edward L. Braun, Joel Armstrong, Dent Earl, 3 1,3 1,3 4 1 Gainesville, FL 32611, USA. Center for Biomolecular Science Ngan Nguyen, Glenn Hickey, Michael W. Vandewege, John A. St. John, § and Engineering, University of California, Santa Cruz, CA Salvador Capella-Gutiérrez,5,6 Todd A. Castoe,7,8 Colin Kern,9 Matthew K. Fujita,8 95064, USA. 4Department of Biochemistry, Molecular 10 11† 11 12 Biology, Entomology and Plant Pathology, Mississippi State Juan C. Opazo, Jerzy Jurka, Kenji K. Kojima, Juan Caballero, 5 12 12 4,13 4 University, Mississippi State, MS 39762, USA. Bioinformatics Robert M. Hubley, Arian F. Smit, Roy N. Platt, Christine A. Lavoie, and Genomics Programme, Centre for Genomic Regulation, Meganathan P. Ramakodi,4,13‡ John W. Finger Jr.,14 Alexander Suh,15,16 08003 Barcelona, Spain. 6Universitat Pompeu Fabra, 08003 7 Sally R. Isberg,17,18,19 Lee Miles,18# Amanda Y. Chong,18 Weerachai Jaratlerdsiri,18 Barcelona, Spain. Department of Biochemistry and 18 18 20 21 Molecular Genetics, University of Colorado School of Jaime Gongora, Christopher Moran, Andrés Iriarte, John McCormack, Medicine, Aurora, CO 80045, USA. 8Department of Biology, Shane C. Burgess,22 Scott V. Edwards,23 Eric Lyons,24 Christina Williams,25 University of Texas, Arlington, TX 76019, USA. 9Department 25 26 13 13,27 of Computer and Information Sciences, University of Matthew Breen, Jason T. Howard, Cathy R. Gresham, Daniel G. Peterson, 10 15 7 3,28 29 Delaware, Newark, DE 19717, USA. Instituto de Ciencias Jürgen Schmitz, David D. Pollock, David Haussler, Eric W. Triplett, Ambientales y Evolutivas, Facultad de Ciencias, Universidad 30,31 32 26 33 Guojie Zhang, Naoki Irie, Erich D. Jarvis, Christopher A. Brochu, Austral de Chile, Valdivia, Chile. 11Genetic Information Carl J. Schmidt,34 Fiona M. McCarthy,35 Brant C. Faircloth,36,37 Federico G. Hoffmann,4,13 Research Institute, Mountain View, CA 94043, USA. 12 Travis C. Glenn,14 Toni Gabaldón,5,6,38 Benedict Paten,3 David A. Ray4,13,39 Institute for Systems Biology, Seattle, WA 98109, USA. * 13Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA. 14Department of Environmental Health Science, To provide context for the diversification of archosaurs—the group that includes University of Georgia, Athens, GA 30602, USA. 15Institute of crocodilians, dinosaurs, and birds—we generated draft genomes of three crocodilians: Experimental Pathology (ZMBE), University of Münster, D-48149 Münster, Germany. 16Department of Evolutionary Alligator mississippiensis (the American alligator), Crocodylus porosus (the saltwater Biology (EBC), Uppsala University, SE-752 36 Uppsala, crocodile), and Gavialis gangeticus (the Indian gharial). We observed an exceptionally Sweden. 17Porosus Pty. Ltd., Palmerston, NT 0831, Australia. slow rate of genome evolution within crocodilians at all levels, including nucleotide 18Faculty of Veterinary Science, University of Sydney, 19 substitutions, indels, transposable element content and movement, gene family evolution, Sydney, NSW 2006, Australia. Centre for Crocodile Research, Noonamah, NT 0837, Australia. 20Departamento and chromosomal synteny. When placed within the context of related taxa including birds de Desarrollo Biotecnológico, Instituto de Higiene, Facultad and turtles, this suggests that the common ancestor of all of these taxa also exhibited slow de Medicina, Universidad de la República, Montevideo, genome evolution and that the comparatively rapid evolution is derived in birds. The data Uruguay. 21Moore Laboratory of Zoology, Occidental College, 22 also provided the opportunity to analyze heterozygosity in crocodilians, which indicates a Los Angeles, CA 90041, USA. College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ 85721, USA.
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