Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs
Structured Abstract
INTRODUCTION
Crocodilians and birds are the two extant clades of archosaurs, a group that includes the extinct dinosaurs and pterosaurs. Fossils suggest that living crocodilians (alligators, crocodiles, and gharials) have a most recent common ancestor 80 to 100 million years ago. Extant crocodilians are notable for their distinct morphology, limited intraspecific variation, and slow karyotype evolution. Despite their unique biology and phylogenetic position, little is known about genome evolution within crocodilians.
RATIONALE
Genome sequences for the American alligator, saltwater crocodile, and Indian gharial—representatives of all three extant crocodilian families—were obtained to facilitate better understanding of the unique biology of this group and provide a context for studying avian genome evolution. Sequence data from these three crocodilians and birds also allow reconstruction of the ancestral archosaurian genome.
RESULTS
We sequenced shotgun genomic libraries from each species and used a variety of assembly strategies to obtain draft genomes for these three crocodilians. The assembled scaffold N50 was highest for the alligator (508 kilobases). Using a panel of reptile genome sequences, we generated phylogenies that confirm the sister relationship between crocodiles and gharials, the relationship with birds as members of extant Archosauria, and the outgroup status of turtles relative to birds and crocodilians.
We also estimated evolutionary rates along branches of the tetrapod phylogeny using two approaches: ultraconserved element–anchored sequences and fourfold degenerate sites within stringently filtered orthologous gene alignments. Both analyses indicate that the rates of base substitution along the crocodilian and turtle lineages are extremely low. Supporting observations were made for transposable element content and for gene family evolution. Analysis of whole-genome alignments across a panel of reptiles and mammals showed that the rate of accumulation of micro-insertions and microdeletions is proportionally lower in crocodilians, consistent with a single underlying cause of a reduced rate of evolutionary change rather than intrinsic differences in base repair machinery. We hypothesize that this single cause may be a consistently longer generation time over the evolutionary history of Crocodylia.
Low heterozygosity was observed in each genome, consistent with previous analyses, including the Chinese alligator. Pairwise sequential Markov chain analysis of regional heterozygosity indicates that during glacial cycles of the Pleistocene, each species suffered reductions in effective population size. The reduction was especially strong for the American alligator, whose current range extends farthest into regions of temperate climates.
CONCLUSION
We used crocodilian, avian, and outgroup genomes to reconstruct 584 megabases of the archosaurian common ancestor genome and the genomes of key ancestral nodes. The estimated accuracy of the archosaurian genome reconstruction is 91% and is higher for conserved regions such as genes. The reconstructed genome can be improved by adding more crocodilian and avian genome assemblies and may provide a unique window to the genomes of extinct organisms such as dinosaurs and pterosaurs.
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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Supplementary Material
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Materials and Methods
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References and Notes
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Science
Volume 346 | Issue 6215
12 December 2014
12 December 2014
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Copyright © 2014, American Association for the Advancement of Science.
Submission history
Received: 7 April 2014
Accepted: 6 November 2014
Published in print: 12 December 2014
Acknowledgments
Genome drafts have been submitted to the National Center for Biotechnology Information repository under the following accession numbers: Alligator mississippiensis, AKHW00000000; Crocodylus porosus, JRXG00000000; Gavialis gangeticus, JRWT00000000. Supplemental files have been archived at GigaScience (DOIs: 10.5524/100125, 10.5524/100126, 10.5524/100127, and 10.5524/100128) and at crocgenomes.org. This project was conducted by the International Crocodilian Genomes Working Group (ICGWG; www.crocgenomes.org). Supported by NSF grants MCB-1052500 and DEB-1020865 (D.A.R.), MCB-0841821 (D.A.R., D.G.P., F.M.M., C.J.S.), DUE-0920151 (E.L.B., E.W.T.), DBI-0905714 (M.K.F.), and DEB-1242260 (B.C.F.). D.A.R., F.M.M., and D.G.P. were also supported by the Institute for Genomics, Biocomputing and Biotechnology at Mississippi State University. S.R.I., L.G.M., J.G., and C.M. were supported by Australian Rural Industries Research and Development Corporation grants (RIRDC PRJ-000549, RIRDC PRJ- 005355, RIRDC PRJ-002461). R.E.G. is a Searle Scholar, Sloan Fellow, and consultant for Dovetail Genomics. E.D.J. was supported by the Howard Hughes Medical Institute and the National Institutes of Health. E.L. received support from the Gordon and Betty Moore Foundation (#3383). R. Elsey, S. Lance, and T. Tuberville aided in collecting alligator samples. The following centers were vital in permitting the computational analyses required for this project: The High Performance Computing Collaborative (HPC2) at Mississippi State University, the High Performance Computing Center at Texas Tech University, the Georgia Advanced Computing Resource Center at the University of Georgia, the University of Florida High Performance Computing Center. The National Institutes of Health provided funding for UCSC infrastructure used in computing whole genome alignments and ancestral genome reconstructions (1U41HG007234-01, 1U41HG006992-2, 5U01HG004695). Finally, we are grateful to K. Vliet and D. Barber for providing access to fresh gharial blood.
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