Genetic analysis of cave bear specimens from Niedźwiedzia cave, sudetes, Poland

Palaeontologia Electronica

Volumn 15, Issue 2, 2012, Pages

  Baca, Mateusz ^a   Stankovic, Anna ^b   Stefaniak, Krzysztof ^c   Marciszak, Adrian ^c   Hofreiter, Michael ^d   Nadachowski, Adam ^e   Wegleński, Piotr ^b   Mackiewicz, Paweł ^c  

^a UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c UNIVERSITY OF WROC AW   (Poland)

^d UNIVERSITY OF YORK   (United Kingdom)

^e INSTITUTE OF SYSTEMATICS AND EVOLUTION OF ANIMALS   (Poland)

Author keywords

Ancient DNA; Cave bear; Phylogeny; Ursus ingressus; Ursus spelaeus

Indexed keywords

BEAR; CAVE; DNA; FOSSIL RECORD; GENETIC ANALYSIS; MORPHOLOGY; NEW RECORD; PHYLOGENY; PLEISTOCENE; SKULL; TAXONOMY; TOOTH;

POLAND; SUDETES;

URSUS; URSUS SPELAEUS;

EID: 84879137121     PISSN: None     EISSN: 10948074     Source Type: Journal    
DOI: 10.26879/301     Document Type: Article

References (65)

1. Bandelt, H.-J., Forster, P., and Röhl, A. 1999. Medianjoining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16:37-48.
2. Baryshnikov, G. 2006. Morphometrical variability of cheek teeth of cave bears, p. 81-102. In Scientific Annals, Vol. 98. School of Geology, Aristotle University of Thessaloniki.
3. Baryshnikov, G. and Puzachenko, A.Y. 2011. Craniometrical variability in the cave bears (Carnivora, Ursidae): Multivariate comparative analysis. Quaternary International, 245:350-368.
4. Baryshnikov, G., Germonpré, M., and Sablin, M. 2003. Sexual dimorphism and morphometric variability of cheek teeth of the cave bears (Ursus spelaeus). Belgian Journal of Zoology, 133:111-119.
5. Bieroński, J., Stefaniak, K., Hercman, H., Socha, P., and Nadachowski, A. 2009. Palaeogeographic and palaeoecological analysis of sediments of the Niedźwiedzia Cave in Kletno, p. 401-422. In Stefaniak, K., Tyc, A., and Socha, P. (eds.), Karst of the Cze{ogonek}stochowa Upland and of the Eastern Sudetes: palaeoenvironments and protection. Studies of the Faculty of Earth Sciences, University of Silesia, No. 56, Sosnowiec-Wrocław.
6. Bocherens, H., Stiller, M., Hobson, K.A., Pacher, M., Rabeder, G., Burns, J.A., Tütken, T., and Hofreiter, M. 2011. Niche partitioning between two sympatric genetically distinct cave bears (Ursus spelaeus and Ursus ingressus) and brown bear (Ursus arctos) from Austria: isotopic evidence from fossil bones. Quaternary International, 245:238-248.
7. Bon, C., Caudy, N., de Dieuleveult, M., Fosse, P., Philippe, M., Maksud, F., Beraud-Colomb, E., Bouzaid, E., Kefi, R., Laugier, C., Rousseau, B., Casane, D., van der Plicht, J., and Elalouf, J.M. 2008. Deciphering the complete mitochondrial genome and phylogeny of the extinct cave bear in the Paleolithic painted cave of Chauvet. Proceedings of the National Academy of Sciences USA, 105:17447-17452.
8. Diedrich, C.G. 2010. Spotted hyena and steppe lion predation behaviours on cave bears of Europe-Late Quaternary cave bear extinction as result of predator stress. Geophysical Research Abstracts, 12.
9. Dotsika, E., Zisi, N., Tsoukala, E., Poutoukis, D., Lykoudis, S., and Giannakopoulos, A. 2011. Palaeo-climatic information from isotopic signatures of Late Pleistocene Ursus ingressus bone and teeth apatite (Loutra Arideas Cave, Macedonia, Greece). Quaternary International, 245:291-301.
10. Guindon, S. and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52:696-704.
11. Hänni, C., Laudet, V., Stehelin, D., and Taberlet, P. 1994. Tracking the origins of the cave bear (Ursus spelaeus) by mitochondrial-DNA sequencing. Proceedings of the National Academy of Sciences USA, 91:12336-12340.
12. Hofreiter, M., Münzel, S., Conard, N.J., Pollack, J., Slatkin, M., Weiss, G., and Pääbo, S. 2007. Sudden replacement of cave bear mitochondrial DNA in the late Pleistocene. Current Biology, 17:R122-R123.
13. Hofreiter, M., Rabeder, G., Jaenicke-Després, V., Withalm, G., Nagel, D., Paunovic, M., Jambrěsić, G., and Pääbo, S. 2004b. Evidence for reproductive isolation between cave bear populations. Current Biology, 14:40-43.
14. Hofreiter, M., Serre, D., Rohland, N., Rebeder, G., Nagel, D., Conrad, N., Münzel, S., and Pääbo, S. 2004a. Lack of phylogeography in European mammals before the last glaciation. Proceedings of the National Academy of Sciences USA, 101:12963-12968.
15. Hofreiter, M., Apelli, C., Krings, M., Waits, L., Conrad, N., Münzel, S., Rabeder, G., Nagel, D., Paunovic, M., Jambrěsić, G., Meyer, S., Weiss, G., and Pääbo, S. 2002. Ancient DNA analyses reveal high mitochondrial DNA sequence diversity and parallel morphological evolution of Late Pleistocene cave bears. Molecular Biology and Evolution, 19:1244-1250.
16. Knapp, M., Rohland, N., Weinstock, J., Baryshnikov, G., Sher, A., Nagel, D., Rabeder, G., Pinhasi, R., Schmidt, H.A., and Hofreiter, M. 2009. First DNA sequences from Asian cave bear fossils reveal deep divergences and complex phylogeographic patterns. Molecular Ecology, 18:1225-1238
17. Kosintsev, P. 2007. Late Pleistocene large mammal faunas from the Urals. Quaternary International, 160:112-120.
18. Krause, J., Unger, T., Noçon, A., Malaspinas, A.S., Kolokotronis, S.O., Stiller, M., Soibelzon, L., Spriggs, H., Dear, P.H., Briggs, A.W., Bray, S.C., O'Brien, S.J., Rabeder, G., Matheus, P., Cooper, A., Slatkin, M., Pääbo, S., and Hofreiter, M. 2008. Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. BMC Evolutionary Biology, 8:220.
19. Krzywicki, T. 2002. The maximum ice sheet limit of the Vistulian Glaciation in northeastern Poland and neighbouring areas. Geological Quarterly, 46:165-188.
20. Kurtén, B. 1968. Pleistocene Mammals of Europe. Aldine Publishing, Chicago.
21. Kurtén, B. 1976. The Cave Bear Story. Life and Death of a Vanished Animal. Columbia University Press, New York.
22. Lartillot, N. and Philippe, H. 2004. A Bayesian mixture model for across site heterogeneities in the aminoacid replacement process. Molecular Biology and Evolution, 21:1095-1109
23. Loreille, O., Orlando, L., Patou-Mathis, M., Philippe, M., Taberlet, P., and Hänni, C. 2001. Ancient DNA analysis reveals divergence of the cave bear, Ursus spelaeus, and brown bear, Ursus arctos, lineages. Current Biology, 11:200-203.
24. Mackiewicz, P., Wiszniowska, T., Olejniczak, A.J., Stefaniak, K., Socha, P., and Nadachowski, A. 2010. Analysis of dental enamel thickness in bears with special attention to Ursus spelaeus and U. wenzensis (=minimus) in comparison to selected representatives of mammals, p. 60-77. In Nowakowski, D. (ed.), Morphology and Systematics of Fossil Vertebrates. DN Publisher, Wrocław.
25. Mazza, P. and Rustioni, M. 1994. On the phylogeny of Eurasian bears. Paleontographica Abteilung A, 230:1-38.
26. Münzel, S.C., Pacher, M., and Athen, K. 2009. Correlating genetic results with biometric analysis on metapodial bones. Slovenský Kras Acta Carsologica Slovaca, 47, Supp. l. 1:47-56.
27. Münzel, S.C., Pacher, M., and Athen, K. 2010. Genetic results versus morphological and biometrical analysis-the Case of Ursus spealaeus (sensu lato). 11th ICAZ International Conference, Paris, 23-28 August 2010, Abstracts of the oral and poster presentations, p. 193.
28. Münzel, S.C., Stiller, M., Hofreiter, M., Mittnik, A., Conard, N.J., and Bocherens, H. 2011. Pleistocene bears in the Swabian Jura (Germany): Genetic replacement, ecological displacement, extinctions and survival. Quaternary International, 245:225-237.
29. Nadachowski, A., Lipecki, G., Stefaniak, K., and Wojtal, P. 2010. Radiocarbon dates on cave bear (Ursus spelaeus) and brown bear (Ursus arctos) from Late Pleistocene of Poland, p. 24. In Bocherens, H. and Pacher, M. (eds.), SSP-4.4-Late Quaternary mammal ecology: insight from new approaches (direct dating, stable isotopes, DNA). European Geosciences Union. General Assembly 2010, Vienna, Austria, 02-07 May 2010
30. Nagel, D., Pronin, K., Rabeder, G., Hofreiter, M., Huijer, W., Kavcik, N., Urbanek, C., Withalm, G., and Orlov, N. 2005. Nerubajskoe, a New Cave Bear Site in the Old Nordmann Territory. Mitteilungen der Kommission für Quartärforschung Österreichische Akademie der Wissenschaften, 14:123-134.
31. Noonan, J.P., Hofreiter, M., Smith, D., Priest, J.R., Rohland, N., Rabeder, G., Krause, J., Detter, J.C., Pääbo, S., and Rubin, E.M. 2005. Genomic sequencing of Pleistocene cave bears. Science, 309:597-599.
32. Orlando, L., Bonjean, D., Bocherens, H., Thenot, A., Argant, A., Otte M., and Hänni, C. 2002. Ancient DNA and the population genetics of cave bears (Ursus spelaeus) through space and time. Molecular Biology and Evolution, 19:1920-1933
33. Pacher, M. and Stuart, A.J. 2009. Extinction chronology and palaeobiology of the cave bear (Ursus spelaeus). Boreas, 38:189-206.
34. Pacher, M., Stuart, A.J., Baryshnikov, G., Stiller, M., Kosintsev, P., and Vorobiev, A. 2009. Cave bears of the Ural Mountains-a survey based on direct radiocarbon dates, aDNA and morphometrical analysis. 15th International Cave Bear Symposium-Spišská Nová Ves, Slovakia, 17th-20th of September 2009, Abstract Book, p. 14-17.
35. Polzin, T. and Daneschmand, S.V. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters, 31:12-20.
36. Posada, D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25:1253-1256.
37. R Development Core Team. 2010. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, URL http:// www.R-project.org
38. Rabeder, G. 1995. Evolutionsniveau und Chronologie der Höhlenbären aus der Gamsulzen-Höhle im Toten Gebirge (Oberösterreich). Mitteilungen der Kommission für Quartärforschung Österreichische Akademie der Wissenschaften, 9:69-81.
39. Rabeder, G. 2004. Die Höhlenbären der Sulzfluh-Höhlen. Vorarlberger Naturschau, 15:103-114.
40. Rabeder, G. and Hofreiter, M. 2004. Der neue Stammbaum der Höhlenbären. Die Höhle, 55:1-19.
41. Rabeder, G. and Withalm, G. 2006. Brown bear remains (Ursidae, Mammalia) from Early Pleistocene cave fillings of Deutsch-Altenburg (Lower Austria). 12th International Cave Bear Symposium Aridea/Loutrá, Macedonia, Greece, Greece: School of Geology, Aristotle University of Thessaloniki, Abstract Book, p. 47-48.
42. Rabeder, G., Hofreiter, M., and Withalm, G. 2004a. The systematic position of the cave bear from Potočka zijalka (Slovenia). Mitteilungen der Kommission für Quartärforschung Österreichische Akademie der Wissenschaften, 13:197-200.
43. Rabeder, G., Nagel, D., and Pacher, M. 2000. Der Höhlenbär. Jan Thorbecke Verlag, Stuttgart.
44. Rabeder, G., Pacher, M., and Withalm, G. 2010. Early Pleistocene bear remains from Deutsch-Altenburg (Lower Austria). Mitteilungen der Kommission für Quartärforschung Österreichische Akademie der Wissenschaften, Band 17, Vienna.
45. Rabeder, G., Debeljak, I., Hofreiter, M., and Withalm, G. 2008. Morphological responses of cave bears (Ursus spelaeus group) to high-alpine habitats. Die Höhle, 59:59-72.
46. Rabeder, G., Hofreiter, M., Nagel, D., and Withalm, G. 2004b. New taxa of a cave bears (Ursidae, Carnivora). Cahiers Scientifiques, Hors série, 2:49-68.
47. Ronquist, F. and Huelsenbeck, J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19:1572-1574
48. Rustioni, M. and Mazza, P. 1992. The genus Ursus in Eurasia: Dispersal events and stratigraphical significance. Rivista Italiana di Paleontologia e Stratigrafia, 98:487-494.
49. Sabol, M. 2005. Cave Bears (Ursidae, Mammalia) from the Trojuholník Cave (Slovakia). Mitteilungen der Kommission für Quartärforschung Österreichische Akademie der Wissenschaften, 14:161-175.
50. Sambrook, J., Frisch, E.F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Lab. Press, Plainview, New York.
51. Sanjuan, R. and Wrobel, B. 2005. Weighted leastsquares likelihood ratio test for branch testing in phylogenies reconstructed from distance measures. Systematic Biology, 54:218-229.
52. Shimodaira, H. and Hasegawa, M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics, 17:1246-1247
53. Stiller, M., Knapp, M., Stenzel, U., Hofreiter, M., and Meyer, M. 2009. Direct multiplex sequencing (DMPS)-a novel method for targeted high-throughput sequencing of ancient and highly degraded DNA. Genome Research, 19:1843-1848
54. Stiller, M., Baryshnikov, G., Bocherens, H., Grandal d'Anglade, A., Hilpert, B., Münzel, S.C., Pinhasi, R., Rabeder, G., Rosendahl, W., Trinkaus, E., Hofreiter, M., and Knapp, M. 2010. Withering away-25,000 years of genetic decline preceded cave bear extinction. Molecular Biology and Evolution, 27:975-978.
55. Svendsen, J.I., Alexanderson, H., Astakhov, V.I., Demidov, I., Dowdeswell, J.A., Funder, S., Gataullin, V., Henriksen, M., Hjort, C., Houmark-Nielsen, M., Hubberten, H.W., Ingólfsson, Ó., Jakobsson, M., Kjær, K.H., Larsen, E., Lokrantz, H., Lunkka, J.P., Lysaa, A., Mangerud, J., Matiouchkov, A., Murray, A., Moeller, P., Niessen, F., Nikolskaya, O., Polyak, L., Saarnisto, M., Siegert, C., Siegert, M.J., Spielhagen, R.F., and Stein, R. 2004. Late Quaternary ice sheet history of northern Eurasia. Quaternary Science Reviews, 23:1229-1271
56. Swofford, D.L. 1998. PAUP. Phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
57. Tsoukala, E., Chatzopoulou, K., Rabeder, G., Pappa, S., Nagel, D., and Withalm, G. 2006. Paleontological and stratigraphical research in Loutra Arideas Bear Cave (Almopia Speleopark, Pella, Macedonia, Greece). Scientific Annals. School of Geology. Aristotle University of Thessaloniki, 98:41-67.
58. Valdiosera, C., García, N., Dalén, L., Smith, C., Kahlke, R.D., Lidén, K., Angerbjörn, A., Arsuaga, J.L., and Götherström, A. 2006. Typing single polymorphic nucleotides in mitochondrial DNA as a way to access Middle Pleistocene DNA. Biology Letters, 2:601-603.
59. Velichko, A. and Spasskaya, I. 2002. Climatic change and the development of landscapes, p. 36-69. In Shahgedanova, M. (ed.), The Physical Geography of Northern Eurasia. Oxford University Press, New York.
60. Velichko, A.A., Faustova, M.A., Gribchenko, Yu N., Pisareva, V., and Sudakova, N.G. 2004. Glaciations of the East European Plain-distribution and chronology, p. 337-354. In Ehlers, J. and Gibbard, P.L. (eds.), Quaternary Glaciations-Extent and Chronology. Part I: Europe. Developments in Quaternary Science 2, Elsevier Science.
61. Velichko, A., Pisareva, V., Morozova, T., Borisova, O., Faustova, M., Gribchenko, Y., Timireva, S., Semenov, V., and Nechaev, V. 2010. Correlation of the glacial and periglacial Pleistocene events in Eastern Europe: lines of attack, p. 188-191. In Titov, V.V. and Tesakov, A.S. (eds.), Quaternary stratigraphy and paleontology of the Southern Russia: connections between Europe, Africa and Asia: Abstracts of the International INQUA-SEQS Conference, Rostovon-Don, June 21-26, 2010
62. Wiszniowska, T. 1976. Niedźwiedź jaskiniowy z Kletna i innych jaskiń Polski. Acta Universitatis Wratislaviensis, 311:1-75.
63. Wiszniowska. T. 1978. Panthera spelaea (Goldfuss) z Jaskini Niedźwiedziej w Kletnie. Acta Universitatis Wratislaviensis, 329:113-141.
64. Wiszniowska, T. 1989. Kopalne szcza{ogonek}tki zwierze{ogonek}ce. In Jahn, A., Kozłowski, S., and Wiszniowska, T. (eds.), Jaskinia Niedźwiedzia w Kletnie-Badania i udoste{ogonek}pnianie, p. 255-279. Zakład Narodowy Ossolińskich, Wydawnictwo Polskiej Akademii Nauk, Wrocław-Warszawa-Kraków-Gdańsk-Łódź.
65. Wiszniowska, T., Bieroński, J., and Pakiet, M. 1996. Paleoekologia Masywu Śnieżnika, p. 47-5. In Jahn, A., Kozłowski, S., and Pulina, M. (eds.), Masyw Śnieżnika-zmiany w środowisku przyrodniczym. Polska Agencja Ekologiczna SA, Wydawnictwa PAE, Warszawa.