A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski's horses

Genome Biology and Evolution

Volumn 3, Issue 1, 2011, Pages 1096-1106

  Goto, Hiroki ^a   Ryder, Oliver A ^b   Fisher, Allison R ^a   Schultz, Bryant ^a   Pond, Sergei L Kosakovsky ^c   Nekrutenko, Anton ^a   Makova, Kateryna D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b INSTITUTE FOR CONSERVATION RESEARCH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mitochondrial DNA; Next generation sequencing; Nuclear DNA; Phylogeny; Wild horse

Indexed keywords

EQUIDAE; EQUUS CABALLUS; EQUUS PRZEWALSKII;

ANIMAL; ARTICLE; CLASSIFICATION; ENDANGERED SPECIES; EVALUATION; FEMALE; GENETIC VARIABILITY; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; HORSE; INBREEDING; MALE; METHODOLOGY; MITOCHONDRIAL GENOME; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; ENDANGERED SPECIES; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; GENOME; GENOME, MITOCHONDRIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HORSES; INBREEDING; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY;

EID: 84856619292     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evr067     Document Type: Article

References (56)

1. Ahrens E, Stranzinger G. 2005. Comparative chromosomal studies of E. caballus (ECA) and E. przewalskii (EPR) in a female F1 hybrid. J Anim Breed Genet. 122(Suppl 1):97-102. (Pubitemid 40482960)
2. Ballou JD. 1994. Population biology. In: Houpt KA, editor. Przewalski's horse: the history and biology of an endangered species. Albany (NY): The State University of New York Press. p. 93-113.
3. Beja-Pereira A, et al. 2004. African origins of the domestic donkey. Science 304:1781. (Pubitemid 38787890)
4. Benirschke K, Malouf N, Low RJ, Heck H. 1965. Chromosome complement: differences between Equus caballus and Equus przewalskii, poliakoff. Science 148:382-383.
5. Bensasson D, Feldman MW, Petrov DA. 2003. Rates of DNA duplication and mitochondrial DNA insertion in the human genome. J Mol Evol. 57:343-354. (Pubitemid 37086678)
6. Bouman I, Bouman J. 1994. The history of the Przewalski's horse. In: Boyd L, Houpt KA, editors. Przewalski's horse: the history and biology of an endangered species. Albany (NY): The State University of New York Press. p. 5-38.
7. Bouman JG, Bos H. 1979. Two symptoms of inbreeding depression in Przewalski horses living in captivity. In: de Boer LEM, Bouman J, Bouman I, editors. Genetics and hereditary diseases of the Przewalski horse. Rotterdam (The Netherlands): Foundation for the Preservation and Protection of the Przewalski horse. p. 165-168.
8. Bowling AT, Ruvinsky A. 2000. Genetic aspects of domestication, breeds, and their origins. In: Bowling AT, Ruvinsky A, editors. The genetics of the horse. Wallingford (UK): CABI Publishing. p. 25-51.
9. Bowling AT, Ryder OA. 1987. Genetic studies of blood markers in Przewalski's horses. J Hered. 78:75-80. (Pubitemid 17114874)
10. Bowling AT, et al. 2003. Genetic variation in Przewalski's horses, with special focus on the last wild caught mare, 231 Orlitza III. Cytogenet Genome Res. 101:226-234. (Pubitemid 38280902)
11. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
12. Flagstad O, Røed KH. 2003. Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences. Evolution 57:658-670. (Pubitemid 36463235)
13. Fleischer RC, Perry EA, Muralidharan K, Stevens EE, Wemmer CM. 2001. Phylogeography of the asian elephant (Elephas maximus) based on mitochondrial DNA. Evolution 55:1882-1892. (Pubitemid 32984006)
14. Forstén A. 1992. Mitochondrial-DNA time-table and the evolution of Equus: comparison of molecular and paleontological evidence. Ann Zool Fennici. 28:301-309.
15. Fridjonsson O, et al. 2011. Detection and mapping of mtDNA SNPs in Atlantic salmon using high throughput DNA sequencing. BMC Genomics 12:179.
16. Gilbert MT, et al. 2008. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science 317:1927-1930. (Pubitemid 47509438)
17. Hedrick PW, Parker KM, Miller EL, Miller PS. 1999. Major histocompat-ibility complex variation in the endangered Przewalski's horse. Genetics 152:1701-1710. (Pubitemid 29370347)
18. Hundertmark KJ, et al. 2002. Mitochondrial phylogeography of moose (Alces alces): late pleistocene divergence and population expansion. Mol Phylogenet Evol. 22:375-387. (Pubitemid 34973426)
19. Ishida N, Oyunsuren T, Mashima S, Mukoyama H, Saitou N. 1995. Mitochondrial DNA sequences of various species of the genus Equus with special reference to the phylogenetic relationship between Przewalskii's wild horse and domestic horse. J Mol Evol. 41:180-188.
20. Jansen T, et al. 2002. Mitochondrial DNA and the origins of the domestic horse. Proc Natl Acad Sci U S A. 99:10905-10910.
21. Kim KI, et al. 1999. Phylogenetic relationships of Cheju horses to other horse breeds as determined by mtDNA D-loop sequence polymorphism. Anim Genet. 30:102-108.
22. Kosakovsky Pond SL, Frost SD. 2005. A simple hierarchical approach to modeling distributions of substitution rates. Mol Biol Evol. 22:223-34. (Pubitemid 40130190)
23. Kosakovsky Pond SL, Muse SV. 2006. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
24. Lau AN, et al. 2009. Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences. Mol Biol Evol. 26:199-208.
25. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
26. Lindgren G, et al. 2004. Limited number of patrilines in horse domestication. Nat Genet. 36:335-336. (Pubitemid 38437253)
27. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. 2003. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 4(12):981-94. (Pubitemid 37474645)
28. Makova KD, Li WH. 2002. Strong male-driven evolution of DNA sequences in humans and apes. Nature 416:624-626. (Pubitemid 34406760)
29. Mohr E, 1959. Das Urwildpferd. Die Neue Brehm-Bü cherei. Wittenberg (Lutherstadt): A. Ziemsen Verlag, p. 144.
30. Myka JL, Lear TL, Houck ML, Ryder OA, Bailey E. 2003. FISH analysis comparing genome organization in the domestic horse (Equus caballus) to that of the Mongolian wild horse (E. przewalskii). Cytogenet Genome Res. 102:222-225. (Pubitemid 38280901)
31. Nielsen R. 2004. Population genetic analysis of ascertained SNP data. Hum Genomics. 1(3):218-224.
32. Oakenfull EA, Lim HN, Ryder OA. 2000. A survey of equid mitochondrial DNA: implications for the evolution, genetic diversity, and conservation of Equus. Conserv Genet. 1:341-355.
33. Oakenfull EA, Ryder OA. 1998. Mitochondrial control region and 12S rRNA variation in Przewalski's horse (Equus przewalskii). Anim Genet. 29:456-459. (Pubitemid 29022652)
34. Outram AK, et al. 2009. The earliest horse harnessing and milking. Science 323:1332-1335.
35. Princée FPG, Zimmerman W, Ryder OA, Dolan JM. 1990. The phenotypic approach I genetic management of Przewalski's horse. In: Seal US, Foose TJ, Lacy RC, Zimmerman W, Ryder OA, Princée FPG, editors. Przewalski's horse draft global conservation plan. Apple Valley (MN): CBSG/SSC/IUCN.
36. Ralls K, Ballou J. 1983. Extinction: lessons from zoos. In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL, editors. Genetics and conservation. San Francisco (CA): The Benjamin/Cummings Publishing Company, Inc. p. 164-184.
37. Roca AL, Georgiadis N, O'Brien SJ. 2005. Cytonuclear genomic dissociation in African elephant species. Nat Genet. 37:96-100. (Pubitemid 40070946)
38. Ryder OA. 1993. Przewalski's horse: prospects for reintroduction into the wild. Conserv Biol. 7:13-15.
39. Ryder OA. 1994. Genetic studies of Przewalski's horses and their impact on conservation. In: Boyd L, Houpt KA, editors. Przewalski's horse: the history and biology of an endangered species. Albany (NY): The State University of New York Press. p. 75-92.
40. Ryder OA, et al. 1984. Genetics of Equus przewalskii Poliakov 1881: analysis of genetic variability in breeding lines, comparison of equid DNAs and a brief description of a cooperative breeding program in North America. Equus 2:207-227.
41. Ryder OA, Wedemeyer EA. 1982. A cooperative breeding program for the Mongolian wild horse, Equus przewalskii, in the United States. Biol Conserv. 22:259-271.
42. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406-425.
43. Sasaki M, Endo H, Yamagiwa D, Yamamoto M, Arishima K, Hayashi Y. 1999. Morphological character of the shoulder and leg skeleton in Przewalski's horse (Equus przewalskii). Ann Anat. 181:403-407. (Pubitemid 29348787)
44. Shimodaira H, Hasegawa M. 1999. Multiple comparisons of Log-likelihoods with applications to phylogenetic inference. Mol Biol Evol. 16:1114-1116. (Pubitemid 29368141)
45. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247. (Pubitemid 33735360)
46. Short RV, Chandley AC, Jones RC, Allen WR. 1974. Meiosis in interspecific equine hybrids II. The Przewalski horse/domestic horse hybrid (Equus przewalskii X E. caballus). Cytogenet Cell Genet. 13:465-478.
47. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 10:512-526. (Pubitemid 23157236)
48. Trifonov VA, et al. 2008. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Res. 16:89-107. (Pubitemid 351294778)
49. Vilà C, et al. 2001. Widespread origins of domestic horse lineages. Science 291:474-477. (Pubitemid 32097069)
50. Volf J, Kus E, Prokopová L. 1991. General studbook of the Przewalski horse (Zoological Garden Prague, Prague, Czech Republic) [cited 2011 Jul 1]. Available from: http://przwhorse.pikeelectronic.com/
51. Wade CM, et al. 2009. Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326: 865-867.
52. Wallner B, Brem G, Müller M, Achmann R. 2003. Fixed nucleotide differences on the Y chromosome indicate clear divergence between Equus przewalskii and Equus caballus. Anim Genet. 34:453-456. (Pubitemid 37491856)
53. Xu S, et al. 2007. High altitude adaptation and phylogenetic analysis of Tibetan horse based on the mitochondrial genome. J Genet Genomics. 34:720-729. (Pubitemid 47247621)
54. Xu X, Arnason U. 1994. The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148:357-362. (Pubitemid 24333700)
55. Yang F, et al. 2003. Karyotypic relationships of horses and zebras: results of cross-species chromosome painting. Cytogenet Genome Res. 102:235-243. (Pubitemid 38280903)
56. Zimmermann W. 1997. Die Bedeutung von Semire-servaten für das EEP Przewalskipferd. Zoo Magazin Nordrhein-Westfalen. 3:70-75.