Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths

Genome Biology

Volumn 12, Issue 5, 2011, Pages

  Enk, Jacob ^a   Devault, Alison ^a   Debruyne, Regis ^a,b   King, Christine E ^a   Treangen, Todd ^c   O'Rourke, Dennis ^d   Salzberg, Steven L ^c   Fisher, Daniel ^e   MacPhee, Ross ^f   Poinar, Hendrik ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c Bldg 142   (United States)

^d UNIVERSITY OF UTAH   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

^f DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COLUMBIAN MAMMOTH; CONTROLLED STUDY; CROSS BREEDING; GENE SEQUENCE; GENETIC VARIABILITY; GENOME; MAMMOTH; MITOCHONDRIAL GENOME; MITOGENOME; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PALEONTOLOGY; PHYLOGENY; ANIMAL; CLASSIFICATION; DNA SEQUENCE; ELEPHANT; EVOLUTION; FOSSIL; GENETICS; GENOMICS; HAPLOTYPE; METHODOLOGY; PHYLOGEOGRAPHY; SOUTH AMERICA; SPECIES EXTINCTION;

ELEPHANTIDAE; MAMMUTHUS COLUMBI; MAMMUTHUS PRIMIGENIUS;

MITOCHONDRIAL DNA;

ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; ELEPHANTS; EXTINCTION, BIOLOGICAL; FOSSILS; GENOME, MITOCHONDRIAL; GENOMICS; HAPLOTYPES; MAMMOTHS; NORTH AMERICA; PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA;

EID: 79957641671     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-5-r51     Document Type: Article

References (67)

1. Maglio V. Origin and evolution of the Elephantidae. Trans Am Phil Soc 1973, 63:31-144.
2. Agenbroad LD. North American Proboscideans: Mammoths: The state of Knowledge, 2003. Quat Int 2005, 126-128:73-92.
3. Harington C. Mammoths, bison and time in North America. Quaternary Dating Methods 1984, 299-309. Amsterdam: Elsevier Science Publications, Mahaney W.
4. Lister A, Bahn PG. Mammoths: Giants of the Ice Age 2007, Berkeley, CA: University of California Press, Revised.
5. Kurtén B, Anderson E. Pleistocene Mammals of North America 1980, New York: Columbia University Press.
6. Lister AM, Sher AV. The origin and evolution of the woolly mammoth. Science 2001, 294:1094-1097. 10.1126/science.1056370, 11691991.
7. Lister AM, Sher AV, van Essen H, Wei G. The pattern and process of mammoth evolution in Eurasia. Quat Int 2005, 126-128:49-64.
8. Shoshani J, Tassy P. Advances in proboscidean taxonomy & classification, anatomy & physiology, and ecology & behavior. Quat Int 2005, 126-128:5-20.
9. Barnes I, Shapiro B, Lister A, Kuznetsova T, Sher A, Guthrie D, Thomas MG. Genetic structure and extinction of the woolly mammoth,Mammuthus primigenius. Curr Biol 2007, 17:1072-1075. 10.1016/j.cub.2007.05.035, 17555965.
10. Gilbert MT, Drautz DI, Lesk AM, Ho SY, Qi J, Ratan A, Hsu CH, Sher A, Dalen L, Gotherstrom A, Tomsho LP, Rendulic S, Packard M, Campos PF, Kuznetsova TV, Shidlovskiy F, Tikhonov A, Willerslev E, Iacumin P, Buigues B, Ericson PG, Germonpre M, Kosintsev P, Nikolaev V, Nowak-Kemp M, Knight JR, Irzyk GP, Perbost CS, Fredrikson KM, Harkins TT, et al. Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes. Proc Natl Acad Sci USA 2008, 105:8327-8332. 10.1073/pnas.0802315105, 2423413, 18541911.
11. Debruyne R, Chu G, King CE, Bos K, Kuch M, Schwarz C, Szpak P, Grocke DR, Matheus P, Zazula G, Guthrie D, Froese D, Buigues B, de Marliave C, Flemming C, Poinar D, Fisher D, Southon J, Tikhonov AN, MacPhee RD, Poinar HN. Out of America: ancient DNA evidence for a new world origin of late quaternary woolly mammoths. Curr Biol 2008, 18:1320-1326. 10.1016/j.cub.2008.07.061, 18771918.
12. Nystrom V, Dalen L, Vartanyan S, Liden K, Ryman N, Angerbjorn A. Temporal genetic change in the last remaining population of woolly mammoth. Proc Biol Sci 2010, 277:2331-2337. 10.1098/rspb.2010.0301, 20356891.
13. Enk JM, Yesner DR, Krossen KJ, Veltre DW, O'Rourke DH. Phylogeographic analysis of the mid-Holocene Mammoth from Qagnax Cave, St. Paul Island, Alaska. Palaeogeog Palaeoclimatol Palaeoecol 2009, 273:184-190.
14. Debruyne R, Poinar HN. Time dependency of molecular rates in ancient DNA data sets, a sampling artifact?. Syst Biol 2009, 58:348-360. 10.1093/sysbio/syp028, 20525589.
15. Ho SY, Phillips MJ, Cooper A, Drummond AJ. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 2005, 22:1561-1568. 10.1093/molbev/msi145, 15814826.
16. MacFadden BJ, Hulbert RC. Calibration of mammoth (Mammuthus) dispersal into North America using rare earth elements of Plio-Pleistocene mammals from Florida. Quat Res 2009, 71:41-48.
17. Gillette DD, Madsen DB. The Columbian mammoth, Mammuthus columbi, from the Wasatch Mountains of central Utah. J Paleontol 1993, 67:669-680.
18. Schaedler JM, Krook L, Wootton JA, Hover B, Brodsky B, Naresh MD, Gillette DD, Madsen DB, Horne RH, Minor RR. Studies of collagen in bone and dentin matrix of a Columbian mammoth (late Pleistocene) of central Utah. Matrix 1992, 12:297-307.
19. Knapp M, Hofreiter M. Next generation sequencing of ancient DNA: requirements, strategies and perspectives. Genes 2010, 1:227-243.
20. Krause J, Dear PH, Pollack JL, Slatkin M, Spriggs H, Barnes I, Lister AM, Ebersberger I, Paabo S, Hofreiter M. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature 2006, 439:724-727. 10.1038/nature04432, 16362058.
21. Paabo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M. Genetic analyses from ancient DNA. Annu Rev Genet 2004, 38:645-679. 10.1146/annurev.genet.37.110801.143214, 15568989.
22. Green RE, Krause J, Ptak SE, Briggs AW, Ronan MT, Simons JF, Du L, Egholm M, Rothberg JM, Paunovic M, Paabo S. Analysis of one million base pairs of Neanderthal DNA. Nature 2006, 444:330-336. 10.1038/nature05336, 17108958.
23. Noonan JP, Hofreiter M, Smith D, Priest JR, Rohland N, Rabeder G, Krause J, Detter JC, Paabo S, Rubin EM. Genomic sequencing of Pleistocene cave bears. Science 2005, 309:597-599. 10.1126/science.1113485, 15933159.
24. Schwarz C, Debruyne R, Kuch M, McNally E, Schwarcz H, Aubrey AD, Bada J, Poinar H. New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains. Nucleic Acids Res 2009, 37:3215-3229. 10.1093/nar/gkp159, 2691819, 19321502.
25. Irwin C, Irwin H, Agogino G. Wyoming muck tells of battle: Ice Age vs. Mammoth. National Geographic Society Magazine 1962, 121.
26. McGrew PO. The Rawlins mammoth. Wyoming Geological Society Guidebook 1961, 315-317.
27. Haynes G. Mammoths, Mastodonts and Elephants 1991, Cambridge University Press.
28. Moore WS. Inferring phylogenies from mtDNA variation - mitochondrial-gene trees versus nuclear-gene trees. Evolution 1995, 49:718-726.
29. Nyakaana S, Arctander P. Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male-biased gene flow. Mol Ecol 1999, 8:1105-1115. 10.1046/j.1365-294x.1999.00661.x, 10447852.
30. Vidya TNC, Sukumar R. Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA. J Ethol 2005, 23:205-210.
31. Vidya TNC, Sukumar R, Melnick DJ. Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants. Proc R Soc B Biol Sci 2009, 276:893-902.
32. Rohland N, Reich D, Mallick S, Meyer M, Green RE, Georgiadis NJ, Roca AL, Hofreiter M. Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants. PLoS Biol 2010, 8:e1000564. 10.1371/journal.pbio.1000564, 3006346, 21203580.
33. Roca AL, Georgiadis N, Pecon-Slattery J, O'Brien SJ. Genetic evidence for two species of elephant in Africa. Science 2001, 293:1473-1477. 10.1126/science.1059936, 11520983.
34. Comstock KE, Georgiadis N, Pecon-Slattery J, Roca AL, Ostrander EA, O'Brien SJ, Wasser SK. Patterns of molecular genetic variation among African elephant populations. Mol Ecol 2002, 11:2489-2498. 10.1046/j.1365-294X.2002.01615.x, 12453234.
35. Grubb P, Groves CP, Dudley JP, Shoshani J. Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2000, 2:1-4.
36. Groves CP, Grubb P. Do Loxodonta cyclotis and L. africana interbreed?. Elephant 2000, 2:4-7.
37. Debruyne R. A case study of apparent controversy between molecular phylogenies: the interrelationships of African elephants. Cladistics 2005, 21:31-50.
38. Roca AL, Georgiadis N, O'Brien SJ. Cytonuclear genomic dissociation in African elephant species. Nat Genet 2005, 37:96-100.
39. Fisher D. Season of death, growth rates, and life history of North American mammoths. Proceedings of the First International Conference on Mammoth Site Studies: 11-13 March 1998 2001, 121-135. Lawrence, KS: University of Kansas, West D.
40. Shoshani J, Tassy P. The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives 1996, Oxford; New York: Oxford University Press.
41. Burbano HA, Hodges E, Green RE, Briggs AW, Krause J, Meyer M, Good JM, Maricic T, Johnson PL, Xuan Z, Rooks M, Bhattacharjee A, Brizuela L, Albert FW, de la Rasilla M, Fortea J, Rosas A, Lachmann M, Hannon GJ, Paabo S. Targeted investigation of the Neandertal genome by array-based sequence capture. Science 2010, 328:723-725. 10.1126/science.1188046, 20448179.
42. Maricic T, Whitten M, Paabo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One 2010, 5:e14004. 10.1371/journal.pone.0014004, 2982832, 21103372.
43. Allendorf FW, Leary RF, Spruell P, Wenburg JK. The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 2001, 16:613-622.
44. Rhymer JM, Simberloff D. Extinction by hybridization and introgression. Annu Rev Ecol Systematics 1996, 27:83-109.
45. McMaster Ancient DNA Centre. , http://socserv.mcmaster.ca/adna/index.htm
46. Service de Systématique Moléculaire of the Muséum national d'Histoire naturelle. {AU query: please confirm that this URL is correct; it was not working when checked}., http://www.mnhn.fr/mnhn/ssm/index.html
47. Institute for Molecular Biology and Biotechnology Laboratory. , http://www.science.mcmaster.ca/mobixlab/
48. Ambry Genetics. , http://www.ambrygen.com/
49. Center for Bioinformatics and Computational Biology. , http://www.cbcb.umd.edu/
50. Integrated DNA Technologies (IDT) SciTools OligoAnalyzer 3.1. , http://www.idtdna.com/analyzer/Applications/OligoAnalyzer/
51. Poinar HN, Schwarz C, Qi J, Shapiro B, Macphee RD, Buigues B, Tikhonov A, Huson DH, Tomsho LP, Auch A, Rampp M, Miller W, Schuster SC. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA. Science 2006, 311:392-394. 10.1126/science.1123360, 16368896.
52. Deagle BE, Eveson JP, Jarman SN. Quantification of damage in DNA recovered from highly degraded samples - a case study on DNA in faeces. Front Zool 2006, 3:11. 10.1186/1742-9994-3-11, 1564134, 16911807.
53. Pop M, Phillippy A, Delcher AL, Salzberg SL. Comparative genome assembly. Brief Bioinform 2004, 5:237-248. 10.1093/bib/5.3.237, 15383210.
54. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol 2004, 5:R12. 10.1186/gb-2004-5-2-r12, 395750, 14759262.
55. Drummond AJAB, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A. Geneious v5.1. , http://www.geneious.com/
56. Phillippy AM, Schatz MC, Pop M. Genome assembly forensics: finding the elusive mis-assembly. Genome Biol 2008, 9:R55. 10.1186/gb-2008-9-3-r55, 2397507, 18341692.
57. Schatz MC, Phillippy AM, Shneiderman B, Salzberg SL. Hawkeye: an interactive visual analytics tool for genome assemblies. Genome Biol 2007, 8:R34. 10.1186/gb-2007-8-3-r34, 1868940, 17349036.
58. Brady A, Salzberg SL. Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models. Nat Methods 2009, 6:673-676. 10.1038/nmeth.1358, 2762791, 19648916.
59. Miller W, Drautz DI, Ratan A, Pusey B, Qi J, Lesk AM, Tomsho LP, Packard MD, Zhao F, Sher A, Tikhonov A, Raney B, Patterson N, Lindblad-Toh K, Lander ES, Knight JR, Irzyk GP, Fredrikson KM, Harkins TT, Sheridan S, Pringle T, Schuster SC. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 2008, 456:387-390. 10.1038/nature07446, 19020620.
60. Public FTP Server at the Broad Institute housing the Loxodonta africana nuclear genome. , http://www.broadinstitute.org/ftp/pub/assemblies/mammals/elephant/loxAfr 3/
61. Public FTP server at CBCB storing various datafiles associated with this manuscript. , ftp://ftp.cbcb.umd.edu/pub/data/mammoth/
62. Rogaev EI, Moliaka YK, Malyarchuk BA, Kondrashov FA, Derenko MV, Chumakov I, Grigorenko AP. Complete mitochondrial genome and phylogeny of Pleistocene mammoth Mammuthus primigenius. PLoS Biol 2006, 4:e73. 10.1371/journal.pbio.0040073, 1360101, 16448217.
63. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256. 10.1093/molbev/msn083, 18397919.
64. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. 10.1186/1471-2148-7-214, 2247476, 17996036.
65. Rohland N, Malaspinas AS, Pollack JL, Slatkin M, Matheus P, Hofreiter M. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol 2007, 5:e207. 10.1371/journal.pbio.0050207, 1925134, 17676977.
66. Rambaut A, Drummond A. Tracer v1.3. , http://tree.bio.ed.ac.uk/software/tracer/
67. FigTree v1.3. , http://tree.bio.ed.ac.uk/software/figtree/