Concordant mitochondrial and microsatellite DNA structuring between Polish lowland and Carpathian Mountain wolves

Conservation Genetics

Volumn 14, Issue 3, 2013, Pages 573-588

  Czarnomska, Sylwia D ^a   Jędrzejewska, Bogumiła ^a   Borowik, Tomasz ^a   Niedziałkowska, Magdalena ^a   Stronen, Astrid V ^a   Nowak, Sabina ^b   Mysłajek, Robert W ^b   Okarma, Henryk ⁱ   Konopiński, Maciej ^c   Pilot, Małgorzata ^d   Śmietana, Wojciech ^c   Caniglia, Romolo ^e   Fabbri, Elena ^e   Randi, Ettore ^e,g   Pertoldi, Cino ^f,g,h   Jędrzejewski, Włodzimierz ^a  

^a MAMMAL RESEARCH INSTITUTE   (Poland)

^b Association for Nature Wolf   (Poland)

^c INSTITUTE OF NATURE CONSERVATION   (Poland)

^d MUSEUM AND INSTITUTE OF ZOOLOGY   (Poland)

^e INSTITUTE FOR ENVIRONMENTAL PROTECTION AND RESEARCH ISPRA   (Italy)

^f AARHUS UNIVERSITY   (Denmark)

^g AALBORG UNIVERSITY   (Denmark)

^h AALBORG ZOO   (Denmark)

ⁱ JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Canis lupus; Eastern Germany; Genetic structure; mtDNA lineages; Non invasive molecular techniques; Nuclear DNA; Poland

Indexed keywords

ANTHROPOGENIC EFFECT; CANID; CARNIVORE; FECES; GENE FLOW; GENETIC DIFFERENTIATION; GENETIC MARKER; GENETIC STRUCTURE; GLACIATION; HABITAT FRAGMENTATION; LOWLAND ENVIRONMENT; MITOCHONDRIAL DNA; MOLECULAR ANALYSIS; MOUNTAIN REGION; NATAL DISPERSAL; PHYLOGEOGRAPHY; POPULATION GENETICS; SUBPOPULATION;

CARPATHIANS; GERMANY; POLAND;

ALCES ALCES; CANIDAE; CANIS FAMILIARIS; CANIS LUPUS; LYNX; LYNX LYNX;

EID: 84877745730     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-013-0446-2     Document Type: Article

References (83)

1. Ansorge H, Kluth G, Hahne S (2006) Feeding ecology of wolves Canis lupus returning to Germany. Acta Theriol 51: 99-106.
2. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11: 155-165.
3. Bhagwat SA, Willis KJ (2008) Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? J Biogeogr 35: 464-482.
4. Blanco JC, Cortes Y (2007) Dispersal patterns, social structure and mortality of wolves living in agricultural habitats in Spain. J Zool 273: 114-124.
5. Blanco JC, Cortes Y, Virgos E (2005) Wolf response to two kinds of barriers in an agricultural habitats in Spain. Can J Zool 83: 312-323.
6. Broquet T, Menard N, Petit E (2007) Nonivasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rate. Conserv Genet 8: 249-260.
7. Carmichael LE, Nagy JA, Larter NC, Strobeck C (2001) Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol Ecol 10: 2787-2798.
8. Ciucci P, Reggioni W, Maiorano L, Boitani L (2009) Long-distance dispersal of a rescued wolf from the northern Apennines to the western Alps. J Wildl Manage 73: 1300-1306.
9. Concise Statistical Yearbook of Poland (2011) Central Statistical Office, Warszawa.
10. Demographic Yearbook of Poland (2011) Central Statistical Office, Warszawa.
11. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571-2581.
12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
13. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3. 0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1: 47-50.
14. Fabbri E, Caniglia R, Mucci N, Thomsen HP, Krag K, Pertoldi C, Loeschcke V, Randi E (2012) Comparison of single nucleotide polymorphisms and microsatellites in non-invasive genetic monitoring of a wolf population. Arch Biol Sci Belgrade 64: 321-335.
15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
16. Forestry (2011) Central Statistical Office, Warszawa.
17. Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7: 359-362.
18. Fuller TK, Mech LD, Cochrane JF (2003) Wolf population dynamics. In: Mech LD, Boitani L (eds) Wolves: behaviour, ecology and conservation. University of Chicago Press, Chicago, pp 161-191.
19. Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile gray wolf. Mol Ecol 13: 2481-2490.
20. Goudet J (1995) FSTAT (version 1. 2): a computer program to calculate F-statistics. J Hered 86: 485-486.
21. Guillot G (2008) Inference of structure in subdivided populations at low levels of genetic differentiation. The correlated allele frequencies model revisited. Bioinformatics 24: 2222-2228.
22. Guillot G, Mortier F, Estoup A (2005) Geneland: a program for landscape genetics. Mol Ecol Notes 5: 712-715.
23. Gursky IG (1985) Ukraine and Moldavia. In: Bibikov DI (ed) The wolf. History, systematics, morphology, ecology. Nauka Publishers, Moskva, pp 487-493 (In Russian).
24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
25. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
26. Hofreiter M, Serre D, Rohland N, Rabeder G, Nagel D, Conard N, Münzel S, Pääbo S (2004) Lack of phylogeography in European mammals before the last glaciations. PNAS 101: 12963-12968.
27. Huck M, Je{ogonek}drzejewski W, Borowik T, Miłosz-Cielma M, Schmidt K, Je{ogonek}drzejewska B, Nowak S, Mysłajek RW (2010) Habitat suitability, corridors and dispersal barriers for large carnivores in Poland. Acta Theriol 55: 177-192.
28. Huck M, Je{ogonek}drzejewski W, Borowik T, Je{ogonek}drzejewska B, Nowak S, Mysłajek RW (2011) Analyses of least cost paths for determining effects of habitat types on landscape permeability: wolves in Poland. Acta Theriol 56: 91-101.
29. Jansson E, Ruokonen M, Kojola I, Aspi J (2012) Rise and fall of wolf population: genetic diversity and structure during recovery, rapid expansion and drastic decline. Mol Ecol 21: 5178-5193.
30. Je{ogonek}drzejewski W, Schmidt K, Theuerkauf J, Je{ogonek}drzejewska B, Okarma H (2001) Daily movements and territory use by radio-collared wolves (Canis lupus) in Białowieża Primeval Forest in Poland. Can J Zool 79: 1993-2004.
31. Je{ogonek}drzejewski W, Niedziałkowska M, Mysłajek RW, Nowak S, Je{ogonek}drzejewska B (2004) Habitat variables associated with wolf (Canis lupus) distribution and abundance in northern Poland. Divers Distrib 10: 225-233.
32. Je{ogonek}drzejewski W, Niedziałkowska M, Mysłajek RW, Nowak S, Je{ogonek}drzejewska B (2005a) Habitat selection by wolves Canis lupus in the uplands and mountains of southern Poland. Acta Theriol 50: 417-428.
33. Je{ogonek}drzejewski W, Branicki W, Veit C, Medugorac I, Pilot M, Bunevich AN, Je{ogonek}drzejewska B, Schmidt K, Theuerkauf J, Okarma H, Gula R, Szymura L, Förster M (2005b) Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus. Acta Theriol 50: 1-22.
34. Je{ogonek}drzejewski W, Je{ogonek}drzejewska B, Zawadzka B, Borowik T, Nowak S, Mysłajek RW (2008) Habitat suitability model for Polish wolves based on long-term national census. Anim Conserv 11: 377-390.
35. Je{ogonek}drzejewski W, Je{ogonek}drzejewska B, Andersone-Lilley Ž, Balčiauskas L, Männil P, Ozoliņš J, Sidorovich VE, Bagrade G, Kübarsepp M, Ornicāns A, Nowak S, Pupila A, Žunna A (2010) Synthesizing wolf ecology and management in eastern Europe: similarities and contrasts with North America. In: Musiani M, Boitani L, Paquet PC (eds) The world of wolves: new perspectives on ecology, behaviour and management. University of Calgary Press, Calgary, pp 207-233.
36. Je{ogonek}drzejewski W, Niedziałkowska M, Hayward MW, Goszczyński J, Je{ogonek}drzejewska B, Borowik T, Bartoń KA, Nowak S, Harmuszkiewicz J, Juszczyk A, Kałamarz T, Kloch A, Koniuch J, Kotiuk K, Mysłajek RW, Ne{ogonek}dzyńska M, Olczyk A, Teleon M, Wojtulewicz M (2012) Prey choice and diet in wolves related to differentiation of ungulate communities and corresponding wolf subpopulations in Poland. J Mamm 33: 1480-1492.
37. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Biochem Genet 10: 149-163.
38. Jombart T, Pontier D, Durfour A-B (2009) Genetic markers in the playground of multivariate analysis. Heredity 102: 330-341.
39. Leonard JA, Vila C, Fox-Dobbs K, Koch PL, Wayne RK, van Valkenburgh B (2007) Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr Biol 17: 1146-1150.
40. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
41. Muñoz-Fuentes V, Darimont CT, Wayne RK, Paquet PC, Leonard JA (2009) Ecological factors drive differentiation in wolves from British Columbia. J Biogeogr 36: 1516-1531.
42. Musiani M, Leonard JA, Cluff HD, Gates CC, Mariani S, Paquet PC, Vilà C, Wayne RK (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. Mol Ecol 16: 4149-4170.
43. Niedziałkowska M, Je{ogonek}drzejewski W, Mysłajek RW, Nowak S, Je{ogonek}drzejewska B, Schmidt K (2006) Environmental correlates of Eurasian lynx occurrence in Poland-large scale census and GIS mapping. Biol Conserv 133: 63-69.
44. Niedziałkowska M, Je{ogonek}drzejewska B, Honnen A-C, Thurid O, Sidorovich VE, Perzanowski K, Skog A, Hartl GB, Borowik T, Bunevich AN, Lang J, Zachos FE (2011) Molecular biogeography of red deer Cervus elaphus from eastern Europe: insights from mitochondrial DNA sequences. Acta Theriol 56: 1-12.
45. Niedziałkowska M, Je{ogonek}drzejewska B, Wójcik JM, Goodman SJ (2012) Genetic structure of red deer population in northeastern Poland in relation to the history of human interventions. J Wildl Manage 76: 1264-1276.
46. Nowak S, Mysłajek RW, Je{ogonek}drzejewska B (2008) Density and demography of wolf Canis lupus population in the western-most part of the Polish Carpathian Mountains, 1996-2003. Folia Zool 57: 392-402.
47. Nowak S, Mysłajek RW, Kłosińska A, Gabryś G (2011) Diet and prey selection of wolves Canis lupus recolonising Western and Central Poland. Mamm Biol 76: 709-715.
48. Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara R et al. (2011) vegan: Community Ecology Package. R package version 2. 0-2.
49. n markers for genetic mapping in the dog. Genomics 16: 207-332.
50. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
51. Pilot M, Je{ogonek}drzejewski W, Branicki W, Sidorovich VE, Je{ogonek}drzejewska B, Stachura K, Funk SM (2006) Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15: 4533-4553.
52. Pilot M, Branicki W, Je{ogonek}drzejewski W, Goszczyński J, Je{ogonek}drzejewska B, Dykyy I, Shkvyrya M, Tsingarska E (2010) Phylogeographic history of grey wolves in Europe. BMC Evol Biol 10: 104.
53. Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
54. Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17: 285-293.
55. Randi E, Lucchini V, Christensen MF, Mucci N, Funk SM, Dolf G, Loeschcke V (2000) Mitochondrial DNA variability in Italian and East European wolves: detecting the consequences of small population size and hybridization. Conserv Biol 14: 464-473.
56. Raymond M, Rousset F (1995) Genepop (version 3. 1): population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
57. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www. R-project. org/.
58. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
59. Sacks BN, Brown SK, Ernest HB (2004) Population structure of California coyotes corresponds to habitat-specific breaks and illuminate species history. Mol Ecol 13: 1265-1275.
60. Sacks BN, Mitchell BR, Williams CL, Ernest HB (2005) Coyote movements and social structure along a cryptic population genetic subdivision. Mol Ecol 14: 1241-1249.
61. Sambrook J, Russel DW (2001) Purification of nucleic acids. In: Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp A8. 9-A8. 10.
62. Savolainen P, Rosen B, Holmberg A, Leitner T, Uhlen M, Lundeberg J (1997) Sequence analysis of domestic dog mitochondrial DNA for forensic use. J Forensic Sci 42: 593-600.
63. Schede J-U, Schumann G, Wersin-Sielaff A (2010) Wölfe in Brandenburg-eine spurensuche im märkischen Sand. Ministerium für Umwelt, Gesundheit und Verbraucherschutz des Landes Brandenburg, Potsdam.
64. Schmidt K, Kowalczyk R, Ozolins J, Männil P, Fickel J (2009) Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic states. Conserv Gen 10: 497-501.
65. Schmidt K, Ratkiewicz M, Konopinski M (2011) The importance of genetic variability and population differentiation in the Eurasian lynx Lynx lynx for conservation, in the context of habitat and climate change. Mamm Rev 41: 112-124.
66. Schmölcke U, Zachos FE (2005) Holocene distribution and extinction of the moose (Alces alces, Cervidae) in Central Europe. Mamm Biol 70: 329-344.
67. n tandem repeat in an intron of the canine von Willebrand factor gene. Anim Gen 25: 112.
68. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extension of the Mantel test of matrix correspondence. Syst Zool 35: 627-632.
69. Stronen AV, Forbes GJ, Paquet PC, Goulet G, Sallows T, Musiani M (2012) Dispersal in a plain landscape: short-distance genetic differentiation in southwestern Manitoba wolves, Canada. Conserv Gen 13: 359-371.
70. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acid Res 24: 3189-3194.
71. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7: 453-464.
72. Thiessen CD (2007) Population structure and dispersal of wolves in the Canadian Rocky Mountains. MSc thesis, Department of Biology, University of Alberta, Edmonton, Canada.
73. Tollefsrud MM, Kissling R, Gugerli F, Johnsen Ø, Skrøppa T, Rachid C, Cheddadi R, van der Knaap WO, Latałowa M, Terhurne-Berson R, Litt T, Geburek T, Brochman C, Sperisen C (2008) Genetic consequences of glacial survival and postglacial colonization in Norway spruce: combined analysis of mitochondrial DNA and fossil pollen. Mol Ecol 17: 4134-4150.
74. Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2: 377-379.
75. Verardi A, Lucchini V, Randi E (2006) Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol Ecol 15: 2845-2855.
76. Vila C, Amorim IR, Leonard JA, Posada D, Castroviejo J, Petrucci-Fonseca F, Crandall KA, Ellegren H, Wayne RK (1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol Ecol 8: 2089-2103.
77. Wabakken P, Sand H, Liberg O, Bjärvall A (2001) The recovery, distribution and population dynamics of wolves on the Scandinavian Peninsula, 1978-1998. Can J Zool 79: 710-725.
78. Wabakken P, Sand H, Kojola I, Zimmermann B, Arnemo JM, Pedersen HC, Liberg O (2007) Multistage, long-range natal dispersal by a global positioning system-collared Scandinavian wolf. J Wildl Manage 71: 1631-1634.
79. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10: 249-256.
80. Wawrzyniak P, Je{ogonek}drzejewski W, Je{ogonek}drzejewska B, Borowik T (2010) Ungulates and their management in Poland. In: Apollonio M, Andersen R, Putman R (eds) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge, pp 223-242.
81. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
82. Wójcik JM, Kawałko A, Marková S, Searle JB, Kotlík P (2010) Phylogeographic signatures of northward post-glacial colonization from high-latitude refugia: a case study of bank voles using museum specimens. J Zool 281: 249-262.
83. Zedrosser A, Dahle B, Swenson JE, Gerstl N (2001) Status and management of the brown bear in Europe. Ursus 12: 9-20.