Unexpected population genetic structure of European roe deer in Poland: An invasion of the mtDNA genome from Siberian roe deer

Molecular Ecology

Volumn 23, Issue 10, 2014, Pages 2559-2572

  Matosiuk, Maciej ^a   Borkowska, Anetta ^a   Świsłocka, Magdalena ^a   Mirski, Paweł ^a   Borowski, Zbigniew ^b   Krysiuk, Kamil ^c   Danilkin, Aleksey A ^d   Zvychaynaya, Elena Y ^d   Saveljev, Alexander P ^e   Ratkiewicz, Mirosław ^a  

^a UNIVERSITY OF BIALYSTOK   (Poland)

^b Department of Forest Ecology Forest Research Institute Raszyn   (Poland)

^c WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^d SEVERTSOV INSTITUTE OF ECOLOGY AND EVOLUTION   (Russian Federation)

^e Federal Agency of the Scientific Organizations   (Russian Federation)

Author keywords

genetic structure; hybridization; mtDNA introgression; phylogenetic discordance; roe deer; species distribution modelling

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; BAYES THEOREM; DEER; DNA SEQUENCE; FEMALE; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; HYBRIDIZATION; MALE; MITOCHONDRIAL GENOME; MOLECULAR GENETICS; MTDNA INTROGRESSION; NUCLEOTIDE SEQUENCE; PHYLOGENETIC DISCORDANCE; PHYLOGENY; PHYLOGEOGRAPHY; POLAND; POPULATION GENETICS; ROE DEER; SPECIES DISTRIBUTION MODELLING;

GENETIC STRUCTURE; HYBRIDIZATION; MTDNA INTROGRESSION; PHYLOGENETIC DISCORDANCE; ROE DEER; SPECIES DISTRIBUTION MODELLING;

ANIMALS; BAYES THEOREM; DEER; DNA, MITOCHONDRIAL; FEMALE; GENETIC MARKERS; GENETICS, POPULATION; GENOME, MITOCHONDRIAL; HAPLOTYPES; HYBRIDIZATION, GENETIC; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; POLAND; SEQUENCE ANALYSIS, DNA;

EID: 84900801979     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12745     Document Type: Article

References (57)

1. Anderson MJ, (2003) DISTLM Forward: A FORTRAN Computer Program to Calculate a Distance-Based Multivariate Analysis for a Linear Model Using Forward Selection. Department of Statistics, University of Auckland, Auckland, New Zealand.
2. Anderson MJ, (2004) DISTLM v.5: A FORTRAN Computer Program to Calculate a Distance-Based Multivariate Analysis for a Linear Model. Department of Statistics, University of Auckland, Auckland, New Zealand.
3. Avise JC, (2004) Molecular Markers, Natural History, and Evolution, 2nd edn. Sinauer Associates, Sunderland, Massachusetts.
4. Baack EJ, Rieseberg LH, (2007) A genomic view of introgression and hybrid speciation. Current Opinion in Genetics & Development, 17, 513-518.
5. Balloux F, Handley LJL, Jombart T, Liu H, Manica A, (2009) Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proceedings of the Royal Society of London, Series B, Biological Sciences, 276, 3447-3455.
6. Boratynski Z, Alves PC, Berto S, Koskela E, Mappes T, Melo-Ferreira J, (2011) Introgression of mitochondrial DNA among Myodes voles: consequences for energetics? BMC Evolutionary Biology, 11, 355.
7. Buggs RJA, (2007) Empirical study of hybrid zone movement. Heredity, 99, 301-312.
8. Cabria MT, Michaux JR, Gõmez-Moliner BJ, et al,. (2011) Bayesian analysis of hybridization and introgression between the endangered European mink (Mustela lutreola) and the polecat (Mustela putorius). Molecular Ecology, 20, 1176-1190.
9. Chan KMA, Levin SA, (2005) Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution, 59, 720-729.
10. Chikuni K, Mori Y, Tabata T, Saito M, Monma M, Kosugiyama M, (1995) Molecular phylogeny based on the kappa-casein and cytochrome b sequences in the mammalian suborder Ruminantia. Journal of Molecular Evolution, 41, 859-866.
11. Crispo E, Moore JS, Lee-Yaw JA, Gray SM, Haller BC, (2011) Broken barriers: human-induced changes to gene flow and introgression in animals. BioEssays, 33, 508-518.
12. Currat M, Ruedi M, Petit RJ, Excoffier L, (2008) The hidden side of invasions: massive introgression by local genes. Evolution, 62, 1908-1920.
13. Danilkin AA, Hewison AJM, (1996) Behavioural Ecology of Siberian and European Roe Deer. Chapman and Hall, London.
14. Derr JN, Hedrick PW, Halbert ND, et al,. (2012) Phenotypic effects of cattle mitochondrial DNA in American bison. Conservation Biology, 26, 1130-1136.
15. Drummond AJ, Suchard MA, Xie D, Rambaut A, (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969-1973.
16. Dupanloup I, Schneider S, Excoffier L, (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 11, 2571-2581.
17. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ, (2011) A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17, 43-57.
18. Excoffier L, (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology, 13, 853-864.
19. Excoffier L, Lischer HEL, (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
20. Excoffier L, Smouse PE, Quattro JM, (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
21. Excoffier L, Foll M, Petit RJ, (2009) Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics, 40, 481-501.
22. Fu YX, (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
23. Gernhard T, (2008) The conditioned reconstruction process. Journal of Theoretical Biology, 253, 769-778.
24. Gleiss HGW, (1967) Unter Robben, Gnus und Tigerschlangen. Chronik des Zoologischen Gartens Breslau 1865-1965. Natura et Patria Verlag, Wedel, Germany.
25. Gonzalez T, Tsytsulina K, (2008) Capreolus pygargus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. www.iucnredlist.org.
26. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
27. Hellborg L, Ellegren H, (2003) Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific DNA. Molecular Ecology, 12, 283-291.
28. Hewison AJM, Danilkin AA, (2001) Evidence for separate specific status of European (Capreolus capreolus) and Siberian (C. pygargus) roe deer. Mammalian Biology, 66, 13-21.
29. Hewitt GM, (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B, 359, 183-195.
30. Innocenti P, Morrow EH, Dowling DK, (2011) Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science, 332, 845-848.
31. Irwin DE, Rubtsov AS, Panov EN, (2009) Mitochondrial introgression and replacement between yellowhammers (Emberiza citrinella) and pine buntings (Emberiza leucocephalos) (Aves: Passeriformes). Biological Journal of the Linnean Society, 98, 422-438.
32. Kalendar R, Lee D, Schulman AH, (2009) FastPCR Software for PCR primer and probe design and repeat search. Genes, Genomes and Genomics, 3, 1-14.
33. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
34. Lorenc H, (2005) Climate Atlas of Poland. Institute of Meteorology and Water Management, Warsaw. [in Polish].
35. Lovari S, Herrero J, Conroy J, et al,. (2008) Capreolus capreolus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. www.iucnredlist.org.
36. McDonald JH, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654.
37. Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC, (2005) Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Molecular Ecology, 14, 2459-2464.
38. Nilsen EB, Gaillard JM, Andersen R, et al,. (2009) A slow life in hell or a fast life in heaven: demographic analyses of contrasting roe deer populations. Journal of Animal Ecology, 78, 585-594.
39. Osada N, Uno Y, Mineta K, Kameoka Y, Takahashi TeraoK, (2010) Ancient genome-wide admixture beyond the current hybrid zone between Macaca fascicularis and M. mulatta. Molecular Ecology, 19, 2884-2895.
40. Pavlov MP, (1999) Akklimatizatsia okhotnich'e-promylovykh zverei i ptits v SSSR. Chast' 3. Kopytnye (Acclimation of game mammals and birds in the Soviet Union: Part 3. Ungulates). Russian Research Institute of Game Management and Fur Farming, Kirov. [in Russian].
41. Petit RJ, Excoffier L, (2009) Gene flow and species delimitation. Trends in Ecology and Evolution, 24, 386-393.
42. Phillips SJ, Anderson RP, Schapire RE, (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231-259.
43. Posada D, (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
44. Pucek Z, (1981) Keys to Vertebrates of Poland. Mammals. Polish Scientific Publishers, Warsaw.
45. Randi E, Pierpaoli M, Danilkin A, (1998) Mitochondrial DNA polymorphism in populations of Siberian and European roe deer (Capreolus pygargus and C. capreolus). Heredity, 80, 429-437.
46. Randi E, Alves PC, Carranza J, Milosevic-Zlatanovic S, Sfougaris A, Mucci N, (2004) Phylogeography of roe deer (Capreolus capreolus) populations: the effects of historical genetic subdivisions and recent nonequilibrium dynamics. Molecular Ecology, 13, 3071-3083.
47. Rogers AR, (1995) Genetic evidence for a Pleistocene population explosion. Evolution, 49, 608-615.
48. Rozen S, Skaletsky H, (1999) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology, 132, 365-386.
49. Runck AM, Matocq MD, Cook JA, (2009) Historic hybridization and persistence of a novel mito-nuclear combination in red-backed voles (genus Myodes). BMC Evolutionary Biology, 9, 114.
50. Smith S, Turbill C, Suchentrunk F, (2010) Introducing mother's curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares. Molecular Ecology, 19, 36-43.
51. Sommer RS, Fahlke JM, Schmolcke U, Benecke N, Zachos FE, (2009) Quaternary history of the European roe deer Capreolus capreolus. Mammal Review, 39, 1-16.
52. Toews DPL, Brelsford A, (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907-3930.
53. Vernesi C, Pecchioli E, Caramelli D, Tiedemann R, Randi E, Bertorelle G, (2002) The genetic structure of natural and reintroduced roe deer (Capreolus capreolus) populations in the Alps and central Italy, with reference to the mitochondrial DNA phylogeography of Europe. Molecular Ecology, 11, 1285-1297.
54. Vorobieva NV, Sherbakov DY, Druzhkova AS, et al,. (2011) Genotyping of Capreolus pygargus fossil DNA from Denisova Cave reveals phylogenetic relationships between ancient and modern populations. PLoS One, 6, e24045.
55. Wood NJ, Phua SH, (1996) Variation in the control region sequence of the sheep mitochondrial genome. Animal Genetics, 27, 25-33.
56. Zvychaynaya EY, Danilkin AA, Kholodova MV, Sipko TP, Berber AP, (2011a) Analysis of the variability of the control region and cytochrome b gene of mtDNA of Capreolus pygargus Pall. Biology Bulletin, 38, 434-439.
57. Zvychaynaya EY, Kiryakulov VM, Kholodova MV, Danilkin AA, (2011b) Roe deer (Capreolus) from Moscow area: analysis of mitochondrial control region polymorphism. Vestnik okhotovedeniya, 8, 168-172. [in Russian with English summary].