Ancient DNA identifies post-glacial recolonisation, not recent bottlenecks, as the primary driver of contemporary mtDNA phylogeography and diversity in Scandinavian brown bears

Diversity and Distributions

Volumn 19, Issue 3, 2013, Pages 245-256

  Bray, Sarah C E ^a   Austin, Jeremy J ^a,b   Metcalf, Jessica L ^a,c   Østbye, Kjartan ^d,e   Østbye, Eivind ^d   Lauritzen, Stein Erik ^f   Aaris Sørensen, Kim ^g   Valdiosera, Cristina ^h   Adler, Christina J ^a,i   Cooper, Alan ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b MUSEUM VICTORIA   (Australia)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF OSLO   (Norway)

^e INLAND NORWAY UNIVERSITY OF APPLIED SCIENCES   (Norway)

^f UNIVERSITY OF BERGEN   (Norway)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

^h INSTITUTO DE SALUD CARLOS III   (Spain)

ⁱ UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Ancient DNA; Bears; Bottleneck; Post glacial recolonisation

Indexed keywords

ANTHROPOGENIC EFFECT; BEAR; CONSERVATION MANAGEMENT; DIVERGENCE; GENETIC STRUCTURE; GENETIC VARIATION; HABITAT CONSERVATION; HOLOCENE; MITOCHONDRIAL DNA; PHYLOGEOGRAPHY; POPULATION BOTTLENECK; POSTGLACIAL; RECOLONIZATION; REFUGIUM; SPECIES DIVERSITY;

DENMARK; ESTONIA; FINLAND; NORWAY; SWEDEN;

URSUS ARCTOS;

EID: 84874198172     PISSN: 13669516     EISSN: 14724642     Source Type: Journal    
DOI: 10.1111/j.1472-4642.2012.00923.x     Document Type: Article

References (67)

1. Aaris-Sørensen, K. (2009) Diversity and dynamics of the mammalian fauna in Denmark throughout the last glacial-interglacial cycle, c. 115-0 kyr BP. Fossils and Strata, 57, 1-59.
2. Anderson, C.N.K., Ramakrishnan, U., Chan, Y.L. & Hadly, E.A. (2005) Serial SimCoal: a population genetic model for data from multiple populations and points in time. Bioinformatics, 21, 1733-1734.
3. Barnes, I., Matheus, P., Shapiro, B., Jensen, D. & Cooper, A. (2002) Dynamics of Pleistocene Population Extinctions in Beringian Brown Bears. Science, 295, 2267-2270.
4. Beaumont, M.A., Zhang, W. & Balding, D.J. (2002) Approximate Bayesian computation in population genetics. Genetics, 162, 2025-2035.
5. Björck, S. (1995) A review of the history of the Baltic Sea, 13.0-8.0 ka BP. Quaternary International, 27, 19-40.
6. Björck, S. (1996) Late Weichselian/Early Preboreal development of the Öresund Strait; a key area for northerly mammal migration. Acta Archaeologica Lundensia: Seriea in 80, 24, 123-134.
7. Björck, S. & Møller, P. (1987) Late Weichselian Environmental History in Southeastern Sweden during the Deglaciation of the Scandinavian Ice Sheet. Quaternary Research, 28, 1-37.
8. Calvignac, S., Hughes, S., Tougard, C., Michaux, J., Thevenot, M., Philippe, M., Hamdine, W. & Hänni, C. (2008) Ancient DNA evidence for the loss of a highly divergent brown bear clade during historical times. Molecular Ecology, 17, 1962-1970.
9. Calvignac, S., Hughes, S. & Hänni, C. (2009) Genetic diversity of endangered brown bear (Ursus arctos) populations at the crossroads of Europe, Asia and Africa. Diversity and Distributions, 15, 742-750.
10. Chan, Y.L., Anderson, C.N.K. & Hadly, E.A. (2006) Bayesian Estimation of the Timing and Severity of a Population Bottleneck from Ancient DNA. PLOS Genetics, 2, e59.
11. Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
12. Davison, J., Ho, S.Y.W., Bray, S.C., Korsten, M., Tammeleht, E., Hindrikson, M., Østbye, K., Østbye, E., Lauritzen, S.-E., Austin, J., Cooper, A. & Saarma, U. (2011) Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species. Quaternary Science Reviews, 30, 418-430.
13. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
14. Edwards, C.J., Suchard, M.A., Lemey, P., Welch, J.J., Barnes, I., Fulton, T.L., Barnett, R., O'Connell, T.C., Coxon, P., Monaghan, N., Valdiosera, C.E., Lorenzen, E.D., Willerslev, E., Baryshnikov, G.F., Rambaut, A., Thomas, M.G., Bradley, D.G. & Shapiro, B. (2011) Ancient hybridization and an Irish origin for the modern polar bear matriline. Current Biology, 21, 1-8.
15. Flagstad, O., Walker, C.W., Vila, C., Sundqvist, A.K., Fernholm, B., Wiig, O., Koyola, I. & Ellegren, H. (2003) Two centuries of the Scandinavian wolf population: patterns of genetic variability and migration during an era of dramatic decline. Molecular Ecology, 12, 869-880.
16. Galbreath, G.J., Groves, C.P. & Waits, L.P. (2007) Genetic resolution of composition and phylogenetic placement of the Isabelline bear. Ursus, 18, 129-131.
17. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gasvuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321.
18. Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4, 1-9.
19. Hänni, C., Laudet, V., Stehelin, D. & 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.
20. Heaton, T.H., Talbot, S.L. & Shields, G.F. (1996) An ice age refugium for large mammals in the Alexander Archipelago, southeastern Alaska. Quaternary Research, 46, 186-192.
21. Hellborg, L., Walker, C.W., Rueness, E.K., Stacy, J.E., Kojola, I., Valdmann, H., Vila, C., Zimmerman, B., Jakobsen, K.S. & Ellegren, H. (2002) Differentiation and levels of genetic variation in northern European lynx (Lynx lynx) populations revealed by microsatellites and mitochondrial DNA analysis. Conservation Genetics, 3, 97-111.
22. Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87-112.
23. Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
24. Hofreiter, M., Jaenicke, V., Serre, D., Von Haeseler, A. & Pääbo, S. (2001) DNA sequences from multiple amplifications reveal artefacts induced by cytosine deamination in ancient DNA. Nucleic Acids Research, 29, 4793-4799.
25. Hofreiter, M., Serre, D., Rohland, N., Rabeder, G., Nagel, D., Conard, N., Munzel, S. & Pääbo, S. (2004) Lack of phylogeography in European mammals before the last glaciation. Proceedings of the National Academy of Sciences USA, 101, 12963-12968.
26. Höss, M., Kohn, M. & Pääbo, S. (1992) Excrement analysis by PCR. Nature, 359, 199.
27. Houmark-Nielsen, M. (1989) The last interglacial-glacial cycle in Denmark. Quaternary International, 3/4, 31-39.
28. Jaarola, M. & Tegelström, H. (1995) Colonization history of north European voles (Microtus agrestis) revealed by mitochondrial DNA. Molecular Ecology, 4, 299-310.
29. Jaarola, M., Tegelström, H. & Fredga, K. (1999) Colonization history in Fennoscandian rodents. Biological Journal of the Linnean Society, 68, 113-127.
30. Jackson, J.V., Talbot, S.L. & Farley, S. (2008) Genetic characterization of Kenai brown bears (Ursus arctos): microsatellite and mitochondrial DNA control region variation in brown bears of the Kenai Peninsula, south central Alaska. Canadian Journal of Zoology, 86, 756-764.
31. Kindberg, J., Swenson, J.E., Ericsson, G., Bellemain, E., Miquel, C. & Taberlet, P. (2011) Estimating population size and trends of the Swedish brown bear Ursus arctos population. Wildlife Biology, 17, 114-123.
32. Kohn, M., Knauer, F., Stoffella, A., Shröder, W. & Pääbo, S. (1995) Conservation genetics of the European brown bear - a study using excremental PCR of nuclear and mitochondrial sequences. Molecular Ecology, 4, 95-103.
33. Korsten, M., Ho, S.Y.W., Davison, J. et al. (2009) Sudden expansion of a single brown bear maternal lineage across northern continental Eurasia after the last ice age: a general demographic model for mammals? Molecular Ecology, 18, 1963-1979.
34. Kumar, S., Tamura, K. & Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150-163.
35. Leonard, J.A. (2008) Ancient DNA applications for wildlife conservation. Molecular Ecology, 17, 4186-4196.
36. Leonard, J.A., Wayne, R.K. & Cooper, A. (2000) Population genetics of Ice Age brown bears. Proceedings of the National Academy of Sciences USA, 97, 1651-1654.
37. Magri, D., Vendramin, G.G., Comps, B., Dupanloup, I., Geburek, T., Gomory, D., Latalowa, M., Litt, T., Paule, L., Roure, J.M., Tantau, I., van der Knaap, W.O., Petit, R.J. & de Beaulieu, J.L. (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist, 171, 199-221.
38. Masuda, R., Murata, K., Aiurzaniin, A. & Yoshida, M.C. (1998) Phylogenetic status of brown bears Ursus arctos of Asia: a preliminary result inferred from mitochondrial DNA control region sequences. Hereditas, 128, 277-280.
39. Masuda, R., Amano, T. & Ono, H. (2001) Ancient DNA analysis of brown bear (Ursus arctos) remains from the archeological site of Rebun Island, Hokkaido, Japan. Zoological Science, 18, 741-751.
40. Masuda, R., Tamura, T. & Takahashi, O. (2006) Ancient DNA analysis of brown bears skulls from a ritual rock shelter site of the Ainu culture at Bihue, central Hokkaido, Japan. Anthropological Science, 114, 211-215.
41. Matsuhashi, T., Masuda, R., Mano, T. & Yoshida, M.C. (1999) Microevolution of the mitochondrial DNA control region in the Japanese brown bear (Ursus arctos) population. Molecular Biology and Evolution, 16, 676-684.
42. Miller, C.R., Waits, L.P. & Joyce, P. (2006) Phylogeography and mitochondrial diversity of extirpated brown bear (Ursus arctos) populations in the contiguous United States and Mexico. Molecular Ecology, 15, 4477-4485.
43. Narain, Y. & Fredga, K. (1996) A hybrid zone between the Hallefors and Uppsala chromosome races of Sorex araneus in central Sweden. Hereditas, 125, 137-145.
44. Naydenov, K., Senneville, S., Beaulieu, J., Tremblay, F. & Bousquet, J. (2007) Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evolutionary Biology, 7, 233.
45. Østbye, E., Lauritzen, S.E., Østbye, K. & Wiig, O. (2006) Holocene brown bear (Ursus arctos L.) from Norwegian caves. Boreas, 35, 296-316.
46. Rambaut, A.. (2007) Tracer v1.4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed May 2011).
47. Saarma, U., Ho, S., Pybus, O., Kaljuste, M., Tumanov, I., Kojola, I., Vorobiev, A., Markov, N., Saveljev, A., Valdmann, H., Lyapunova, E., Abramov, A., Männil, P., Korsten, M., Vulla, E., Pazetnov, S., Pazetnov, V., Putchkovskiy, S. & Rõkov, A. (2007) Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages. Molecular Ecology, 16, 401-413.
48. Schneider, S., Roessli, D. & Excoffier, L.. (2000) Arlequin: A Software for Population Genetics Analysis. University of Geneva, Geneva.
49. Servheen, C. (1990) The status and conservation of the bears of the world. International Conference of Bear Research and Management Monography Series, 2, 1-32.
50. Siivonen, L. (1982) The history of the Fennoscandian mammal fauna. Acta Zoologica Fennica, 169, 7-10.
51. Sommer, R.S. & Benecke, N. (2005) The recolonization of Europe by brown bears Ursus arctos Linnaeus, 1758 after the Last Glacial Maximum. Mammal Review, 35, 156-164.
52. Sørensen, O.J. (1990) The brown bear in Europe in the mid 1980's. Aquilo Series Zoologica, 27, 3-16.
53. Stewart, J.R. & Lister, A.M. (2001) Cryptic northern refugia and the origins of the modern biota. TRENDS in Ecology and Evolution, 16, 608-613.
54. Swenson, J.E., Wabakken, F., Sandegren, F., Bjarvall, A., Franzen, R. & Soderberg, A. (1995) The near extinction and recovery of brown bears in Scandinavia in relation to the bear management policies of Norway and Sweden. Wildlife Biology, 1, 11-25.
55. Swenson, J.E., Taberlet, P. & Bellemain, E. (2011) Genetics and conservation of European brown bears Ursus arctos. Mammal Review, 41, 87-98.
56. Taberlet, P. & Bouvet, J. (1994) Mitochondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear Ursus arctos in Europe. Proceedings of the Royal Society B: Biological Sciences, 255, 195-200.
57. Taberlet, P., Swenson, J.E. & Sandegren, F. (1995) Localization of a Contact Zone between Two Highly Divergent Mitochondrial DNA Lineages of the Brown Bear Ursus arctos in Scandinavia. Conservation Biology, 9, 1255-1261.
58. Taberlet, P., Fumagalli, L., Wust-Saucy, A. & Cosson, J. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453-464.
59. Tegelström, H. (1987) Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus). Journal of Molecular Evolution, 24, 218-227.
60. Valdiosera, C., Garcia, N., Anderung, C., Dalen, L., Cregut-Bonnoure, E., Kahlke, R.-D., Stiller, M., Brandstrom, M., Thomas, M.G., Arsuaga, J.L. & Götherström, A. (2007) Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Molecular Ecology, 16, 5140-5148.
61. Valdiosera, C., Garcia-Garitagoitia, J.L., Garcia, N., Doadrio, I., Thomas, M.G., Hänni, C., Arsuaga, J.-L., Barnes, I., Hofreiter, M., Orlando, L. & Götherström, A. (2008) Surprising migration and population size dynamics in ancient Iberian brown bears (Ursus arctos). Proceedings of the National Academy of Sciences USA, 105, 5123-5128.
62. Waits, L.P., Talbot, S.L., Ward, R.H. & Shields, G.F. (1998) Mitochondrial DNA phylogeography of the North American brown bear and implications for conservation. Conservation Biology, 12, 408-417.
63. Waits, L.P., Taberlet, P., Swenson, J.E., Sandegren, F. & Franzen, R. (2000) Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Molecular Ecology, 9, 421-431.
64. Walker, C.W., Vila, C., Landa, A., Linden, M. & Ellegren, H. (2001) Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations. Molecular Ecology, 10, 53-63.
65. Willerslev, E. & Cooper, A. (2005) Ancient DNA. Proceedings of the Royal Society B: Biological Sciences, 272, 3-16.
66. Willis, K.J. & van Andel, T.H. (2004) Trees or no trees? The environments of central and eastern Europe during the last glaciation. Quaternary Science Reviews, 23, 2369-2387.
67. Willis, K.J., Rudner, E. & Sumegi, P. (2000) The full-glacial forests of central and southeastern Europe. Quaternary Research, 53, 203-213.