Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

doi:10.1126/science.1254449

. 2014 Dec 12;346(6215):1254449.

doi: 10.1126/science.1254449. Epub 2014 Dec 11.

Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

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.

PMID: 25504731
PMCID: PMC4386873
DOI: 10.1126/science.1254449

Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

Richard E Green et al. Science. 2014.

. 2014 Dec 12;346(6215):1254449.

doi: 10.1126/science.1254449. Epub 2014 Dec 11.

Authors

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.

PMID: 25504731
PMCID: PMC4386873
DOI: 10.1126/science.1254449

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.

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Figures

**Figure 1. Rates of substitution for ultraconserved elements (UCEs) and fourfold degenerate (4D) sites**
(A) Inferred amniote phylogeny based on maximum likelihood analysis of partitioned UCE-anchored loci using RAxML v7.3.4 (17). All branches received 100% bootstrap support. Colors indicate the estimated rates, with cooler colors corresponding to lower rates of molecular evolution (key presented as an insert). (B) Estimated rates of molecular evolution for UCE-anchored loci (left) and 4D sites (right). Red dots indicate the estimated rate for the branch ancestral to the group of interest. The UCE rate for mouse is an outlier; it is indicated by the black dot.

**Figure 2. Rates of substitution, micro-indel and break-point evolution**
(A) 4D, transposable element and, for comparison, UCE rates, measured as subs/site. (B) Indel rate vs. 4D subs/site for each extant lineage. (C) Gene syteny breakage rate vs. 4D subs/site distance from the gene annotated species (either alligator or chicken).

**Figure 3. Relative TE numbers among aminotes**
Shown are TE copies that predate the speciation of crocodilians and mammals in 16 amniote genomes. The figure displays, on a log scale, 55 unrelated TE families present in all amniote genomes, the bases identified in each individual genome relative to the average identified in all 16 genomes. A * indicates that two or more subfamilies were combined to form a single category. See the Supplemental Materials (17) for the full analysis encompassing all 74 TE families.

**Figure 4. OR expansions/contractions within archosaurs**
Subtrees from neighbor-joining phylogenies of the intact crocodilian (A), avian (B) and testudine (C) OR repertoires. Crocodiles are represented by the saltwater crocodile, gharial and American alligator; birds are represented by chicken and zebra finch; and testudines are represented by the soft shell and green sea turtle. Note the paucity of lineage-specific clades, in color, among crocodilian ORs, as opposed to avian and testudine ORs. Most crocodilian ORs are outparalogs, groups of paralogous genes that emerged prior to the divergence of the species analyzed, whereas the vast majority of avian and testudine ORs fall on monophyletic groups of inparalogs, groups of paralogous genes the emerged after the divergence of the species analyzed. Neighbor-joining trees were inferred using MEGA v5, a Poisson model of substitution, and 1000 bootstrap iterations were performed to evaluate support. Also see Figure S24

**Figure 5. Crocodilian genetic diversity and population history**
A. The rate of observed heterozygosity within annotated exons, intergenic sequence, and introns. B. PSMC estimates of the historical crocodilian Ne inferred from each genome shown in a time span of (B) 5 million years and (C) 1 million years under the assumption of a generation time of 20 years.

**Figure 6. Analyzing the archosaur assembly**
A. Expected base reconstruction accuracy B. Total archosaur bases assembled in several annotated functional classes and the number of bases in each category from the alligator genome.

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References

1. Janke A, Arnason U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles) Mol Biol Evol. 1997 Dec;14:1266. - PubMed
1. Sennikov AG. The first ctenosauriscid (Reptilia: Archosauromorpha) from the Lower Triassic Of Eastern Europe. Paleontol J. 2012 Sep 01;46:499.
1. Brochu CA. Phylogenetic approaches toward crocodylian history. Annual Review of Earth and Planetary Sciences. 2003;31:357.
1. Grigg G, Seebacher F, Franklin CE, editors. Crocodilian Biology and Evolution. Surrey, Beatty and Sons, Chipping Norton; NSW: 2001.
1. Cohen MM, Gans C. The chromosomes of the order Crocodilia. Cytogenetics. 1970;1970:81. - PubMed

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[1] Janke A, Arnason U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles) Mol Biol Evol. 1997 Dec;14:1266. - PubMed

[2] Janke A, Arnason U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles) Mol Biol Evol. 1997 Dec;14:1266. - PubMed

[3] Sennikov AG. The first ctenosauriscid (Reptilia: Archosauromorpha) from the Lower Triassic Of Eastern Europe. Paleontol J. 2012 Sep 01;46:499.

[4] Sennikov AG. The first ctenosauriscid (Reptilia: Archosauromorpha) from the Lower Triassic Of Eastern Europe. Paleontol J. 2012 Sep 01;46:499.

[5] Brochu CA. Phylogenetic approaches toward crocodylian history. Annual Review of Earth and Planetary Sciences. 2003;31:357.

[6] Brochu CA. Phylogenetic approaches toward crocodylian history. Annual Review of Earth and Planetary Sciences. 2003;31:357.

[7] Grigg G, Seebacher F, Franklin CE, editors. Crocodilian Biology and Evolution. Surrey, Beatty and Sons, Chipping Norton; NSW: 2001.

[8] Grigg G, Seebacher F, Franklin CE, editors. Crocodilian Biology and Evolution. Surrey, Beatty and Sons, Chipping Norton; NSW: 2001.

[9] Cohen MM, Gans C. The chromosomes of the order Crocodilia. Cytogenetics. 1970;1970:81. - PubMed

[10] Cohen MM, Gans C. The chromosomes of the order Crocodilia. Cytogenetics. 1970;1970:81. - PubMed

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Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

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Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

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