Ancient and contemporary DNA sheds light on the history of Mouse-eared bats in europe and the caucasus

Acta Chiropterologica

Volumn 11, Issue 2, 2009, Pages 289-305

  Bogdanowicz, Wiesław ^a   Van Den Bussche, Ronald A ^b   Gajewska, Marta ^a   Postawa, Tomasz ^c   Harutyunyan, Margarita ^d  

^a MUSEUM AND INSTITUTE OF ZOOLOGY   (Poland)

^b OKLAHOMA STATE UNIVERSITY   (United States)

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

^d RUSSIAN ARMENIAN UNIVERSITY   (Armenia)

Author keywords

Ancient DNA; Europe; Hybridization; Migratory routes; Mouse eared bats; MtDNA and nDNA; Myotis spp.; Refugia

Indexed keywords

BAT; GENETIC DIFFERENTIATION; HYBRIDIZATION; MITOCHONDRIAL DNA; PHYLOGENETICS; PHYLOGEOGRAPHY; POPULATION GENETICS; SUBFOSSIL; SUBSPECIES; TAXONOMY;

CARPATHIANS; EUROPE;

ANIMALIA; MYOTIS; MYOTIS MYOTIS;

EID: 77249178416     PISSN: 15081109     EISSN: None     Source Type: Journal    
DOI: 10.3161/150811009X485530     Document Type: Article

References (86)

1. AHLEN, I., and H. J. BAAGOE. 1999. Use of ultrasound detectors for bat studies in Europe - experiences from field identification, surveys and monitoring. Acta Chiropterologica, 1: 137-150.
2. ALVES, P. C., N. FERRAND, F. SUCHENTRUNK, and D. J. HARRIS. 2003. Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula. Molecular Phylogenetics and Evolution, 27: 70-80.
3. ARLETTAZ, R. 1995. Ecology of the sibling mouse-eared bats (My otis myotis and Myotis blythii): zoogeography, niche, com petition, and foraging. Hours Publishers, Martingy, Va -lais, 208 pp.
4. ARLETTAZ, R. 1999. Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. Journal of Animal Ecology, 68: 460-471.
5. BACHANEK, J. 2008. The northern distribution limits of the lesser mouse-eared bat Myotis oxygnathus (Chiroptera: Vesper -tilionidae) in Central Europe. Acta Zoologica Cracoviensia, 51A(1-2): 59-64.
6. BAKER, R. J., and R. D. BRADLEY. 2006. Speciation in mammals and the genetic species concept. Journal of Mammal -ogy, 87: 643-662.
7. BANDELT, H.-J., P. FORSTER, and A. ROHL. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16: 37-48.
8. BARNES, I., P. MATHEUS, B. SHAPIRO, D. JENSEN, and A. COOPER. 2002. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science, 295: 2267-2270.
9. BENDA, P. 1994. Biometrics of Myotis myotis and Myotis blythi: age variation and sexual dimorphism. Folia Zoologica, 43: 297-306.
10. BENDA, P., and I. HORAEK, 1995a. Biometrics of Myotis myotis and Myotis blythi. Myotis, 32-33: 45-55.
11. BENDA, P., and I. HORAEK. 1995b. Geographic variation in three species of Myotis (Mammalia: Chiroptera) in South of the Western Palearctics. Acta Societatis Zoologicae Bo he -mi cae, 59: 17-39.
12. BERTHIER, P., L. EXCOFFIER, and M. RUEDI. 2006. Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Pro ceedings of the Royal Society of London, 273B: 3101-3109.
13. BILGIN, R., A. FURMAN, E. CORAMAN, and A. KARATA. 2008. Phylogeography of the Mediterranean horseshoe bat, Rhi no lophus euryale (Chiroptera: Rhinolophidae), in southeastern Europe and Anatolia. Acta Chiropterologica, 10: 41-49.
14. BILGIN, R., E. CORAMAN, A. KARATA, and J. C. MORALES. 2009. Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae), in southeastern Europe and Anatolia, with a specific focus on whether the Sea of Marmara is a barrier to gene flow. Acta Chiro pte -rologica, 11: 53-60.
15. BRADLEY, R. D., and R. J. BAKER. 2001. A test of the genetic species concept: cytochrome-b sequences and mammals. Jour nal of Mammalogy, 82: 960-973.
16. CASTELLA, V., M. RUEDI, L. EXCOFFIER, C. IBANEZ, R. ARLET -TAZ, and J. HAUSSER. 2000. Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vesper -tilionidae)? Molecular Ecology, 9: 1761-1772.
17. CASTELLA, V., M. RUEDI, and L. EXCOFFIER. 2001. Contrasted patterns in the mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. Journal of Evol -utionary Biology, 14: 708-720.
18. COOPER, S. J. B., P. R. DAY, T. B. REARDON, and M. SCHULZ. 2001. Assessment of species boundaries in Australian Myotis (Chiroptera: Vespertilionidae) using mitochondrial DNA. Journal of Mammalogy, 82: 328-338.
19. DIETZ, C., and O. VON HELVERSEN. 2004. Illustrated identification key to the bats of Europe, electronic publication, version 1.0. released 15.12.2004. Available at: http://public. carnet.hr/speleo/znanost/sismisi/Dietz-von- Helversen-2004IDkey-1.pdf and http://public.carnet.hr/speleo/znanost/sismisi/ Dietz-von-Helversen-2004IDkey-2.pdf
20. DIETZ, C., O. VON HELVERSEN, and D. NILL. 2007. Handbuch der Fledermause Europas und Nordwestafrikas. Kosmos Verlag, Stuttgart, 399 pp.
21. DUBEY, S., M. ZAITSEV, J. F. COSSON, A. ABDUKADIER, and P. VOGEL. 2006. Pliocene and Pleistocene diversification and multiple refugia in a Eurasian shrew (Crocidura suaveolens group). Molecular Phylogenetics and Evolution, 38: 635-647.
22. DZEVERIN, I. 2008. The stasis and possible patterns of selection in evolution of a group of related species from the bat genus Myotis (Chiroptera, Vespertilionidae). Journal of Mammal -ian Evolution, 15: 123-142.
23. EVIN, A., M. BAYLAC, M. RUEDI, M. MUCEDDA, and J.-M. PONS. 2008. Taxonomy, skull diversity and evolution in a species complex of Myotis (Chiroptera: Vespertilionidae): a geometric morphometric appraisal. Biological Journal of the Linnean Society, 95: 529-538.
24. FELTEN, H., F. SPITZENBERGER, and G. STORCH. 1977. Zur Klein -saugerfauna West-Anatoliens. Teil IIIa. Senckenberg iana Bio logica, 58: 1-44.
25. FOREJT, J. 1996. Hybrid sterility in the mouse. Trends in Gen e t ics, 12: 412-417.
26. FURMAN, A., E. CORAMAN, R. BILGIN, and A. KARATA. 2009. Molecular ecology and phylogeography of the bent-wing bat complex (Miniopterus schreibersii) (Chiroptera: Ves per -ti lionidae) in Asia Minor and adjacent regions. Zoologica Scripta, 38: 129-141.
27. GHAZALI, M. A. 2009. Identification of Myotis blythii and M. my otis (Chiroptera, Vespertilionidae) from eastern Europe based on the measurements of lower teeth. Vestnik Zoologii, 43: 403-408.
28. GIBBARD, P., and T. VON KOLFSCHOTEN. 2004. The Pleistocene and Holocene epochs. Pp. 441-452, in A geologic time scale 2004 (F. M. GRADSTEIN, J. G. OGG, and A. G. SMITH, eds.). Cambridge University Press, Cambridge, 589 pp.
29. GOSLAR, T., and J. CZERNIK. 2000. Sample preparation in the Gliwice radiocarbon laboratory for AMS C14 dating of sediments. Geochronometria, 18:1-8.
30. GOMEZ, A., and D. H. LUNT. 2007. Historial biogeography and conservation of the golden-striped salamander (Chioglossa lusitanica) in northwestern Iberia: integrating ecological, phenotypic and phylogeographic data. Pp. 155-188, in Phy lo geography of southern European refugia - evolutionary perspectives on the origins and conservation of Euro -pean biodiversity (S. WEISS and N. FERRAND, eds.). Sprin -ger, New York, 377 pp.
31. GUNDUZ, I., M. JAAROLA, C. TEZ, C. YENIYURT, P. D. POLLY, and J. B. SEARLE. 2007. Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Scuiridae, Ro -den tia) in Turkey, with a description of a new species. Mo -lec ular Phylogenetics and Evolution, 43: 916-935.
32. HEWITT, G. M. 2004. The structure of biodiversity - insights from molecular phylogeography. Frontiers in Zoology, 1: 4. doi:10.1186/1742-9994-1-4. (Pubitemid 44969272)
33. HORAEK, I. 1984. Remarks on causality of population decline in European bats. Myotis, 21-22: 138-147.
34. HORAEK, I., V. HANAK, and J. GAISLER. 2000. Bats of the Palearctic region: a taxonomic and biogeographic review. Volume 1. Pp. 11-57, in Proceedings of the VIIIth Euro pean Bat Research Sym posium (B. W. WO?OSZYN, ed.). Chiro-pterological Information Cen ter, Krakow, 273 pp.
35. HUELSENBECK, J. P., and B. RANNALA B. 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science, 276: 227-232.
36. HULVA, P., I. HORAEK, P. P. STRELKOV, and P. BENDA. 2004. Mo lecular architecture of Pipistrellus pipistrellus/Pipi strel lus pygmaeus complex (Chiroptera: Vespertilionidae): further cryptic species and Mediterranean origin of the diver gence. Molecular Phylogenetics and Evolution, 32: 1023-1035.
37. HUTTERER, R., T. IVANOVA, C. MEYER-CORDS, and L. RODRI -GUES. 2005. Bat migrations in Europe: a review of banding data and literature. Naturschutz und Biologische Vielfalt, 28: 1-162.
38. IBANEZ, C., J. L. GARCIA-MUDARRA, M. RUEDI, B. STADELMANN, and J. JUSTE. 2006. The Iberian contribution to cryptic diversity in European bats. Acta Chiropterologica, 8: 277-297.
39. IUCN. 2009a. Myotis blythii. In IUCN Red List of Threatened Species. Version 2009.2. http://www.iucnredlist.org. Down -loaded on 9 November 2009.
40. IUCN. 2009b. Myotis myotis. In IUCN Red List of Threatened Species. Version 2009.2. http://www.iucnredlist.org. Down -loaded on 9 November 2009.
41. KAWAI, K., M. NIKAIDO, M. HARADA, S. MATSUMURA, L.-K. LIN, Y. WU, M. HASEGAWA, and N. OKADA. 2003. The status of the Japanese and East Asian bats of the genus Myotis (Ves -per tilionidae) based on mitochondrial sequences. Molec ular Phylogenetics and Evolution, 28: 297-307.
42. KIMURA, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Ecology, 16: 111-120.
43. KOTLIK, P., V. DEFFONTAINE, S. MASCHERETTI, J. ZIMA, J. P. MICHAUX, and J. B. SEARLE. 2006. A northern glacial refu -gium for bank voles (Clethrionomys glareolus). Proceed -ings of the National Academy of Sciences of the USA, 103: 14860-14864.
44. KRYŠTUFEK, B., E. V. BUZAN, W. F. HUTCHINSON, and B. HAN -FLING. 2007. Phylogeography of the rare Balkan endemic Mar tino's vole, Dinaromys bogdanovi, reveals strong differentiation within the western Balkan Peninsula. Molecular Ecology, 16: 1221-1232.
45. LEONARD, J. A., R. K. WAYNE, J. WHEELER, R. VALADEZ, S. GUILLEN, and C. VILA. 2002. Ancient DNA evidence for Old World origin of New World dogs. Science, 298: 1613-1616.
46. LEONARD, J. A., C. VILA, and R. K. WAYNE. 2005. Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus). Molecular Ecology, 14: 9-17.
47. LEONARD, J. A., C. VILA, K. FOX-DOBBS, P. L. KOCH, R. K. WAYNE, and B. VAN VALKENBURGH. 2007. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Current Biology, 17: 1146-1150.
48. LEWONTIN, R. C. 1974. The genetic basis of evolutionary change. Columbia University Press, New York, 346 pp.
49. MADDISON, W. P., and D. R. MADDISON. 2000. MacClade, version 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA.
50. MAGRI, D., G. C. VENDRAMIN, B. COMPS, I. DUPANLOUP, T. GEBUREK, D. GOMORY, M. LATAOWA, et al. 2006. A new scenario for the Quaternary history of European beechpopulations: palaeobotanical evidence and genetic consequences. New Phytologist, 171: 199-221.
51. MAYER, F., C. DIETZ, and A. KIEFER. 2007. Molecular species identification boosts bat diversity. Frontiers in Zoology, 4: 4. doi:10.1186/1742-9994-4-4. (Pubitemid 46321373)
52. MAYER, F., and O. VON HELVERSEN. 2001. Cryptic diversity in European bats. Proceedings of the Royal Society of London, 268: 1825-1832.
53. MICHAUX, J. R., R. LIBOIS, E. PARADIS, and M. G. FILIPPUCCI. 2004. Phylogeographic history of the yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Molecular Phylogenetics and Evolution, 32: 788-798.
54. MITCHELL-JONES,A. J., G. AMORI, W. BOGDANOWICZ, B. KRYŠ -TUFEK, P. J. H. REIJNDERS, F. SPITZENBERGER, M. STUBBE, J. B. M. THISSEN, V. VOHRALIK, and J. ZIMA. 1999. The atlas of European mammals. Academic Press, London, 484 pp.
55. PEREIRA, M. J. R., H. REBELO, A. RAINHO, and J. M. PALMEIRIM. 2002. Prey selection by Myotis myotis (Vespertilionidae) in a Mediterranean region. Acta Chiropterologica, 4: 183-193.
56. PETIT, E., L. EXCOFFIER, and F. MAYER. 1999. No evidence of bottleneck in the postglacial recolonization of Europe by the noctule bat (Nyctalus noctula). Evolution, 53, 1247-1258.
57. PETIT, R. J., I. AGUINAGALDE, J.-L. DE BEAULIEU, C. BITTKAU, S. BREWER, R. CHEDDADI, R. ENNOS, et al. 2003. Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300: 1563-1565.
58. PIAGGIO, A. J., and S. L. PERKINS, 2005. Molecular phylogeny of North American long-eared bats (Vespertilionidae: Cory -nor hinus): inter- and intraspecific relationships inferred from mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 37: 762-775.
59. PIDANCIER, N., S. JORDAN, G. LUIKART, and P. TABERLET. 2006. Evolutionary history of the genus Capra (Mammalia, Artio -dactyla): discordance between mitochondrial DNA and Ychromosome phylogenies. Molecular Phylogenetics and Evo l ution, 40: 739-749.
60. POPOV, V. V. 2004. Pliocene small mammals (Mammalia, Lipo -typhla, Chiroptera, Lagomorpha, Rodentia) from Muselievo (North Bulgaria). Geodiversitas, 26: 403-491.
61. POSADA, D., and K. A. CRANDALL. 1998. ModelTest: testing the model of DNA substitution. Bioinformatics, 14:817-818.
62. POSTAWA, T. 2004. Changes in bat fauna during the Middle and Late Holocene as exemplified by thanatocoenoses dated with 14C AMS from Krakow-Cz?stochowa Upland caves (Poland). Acta Chiropterologica, 6: 269-292.
63. PRAGER, E. M., C. ORREGO, and R. D. SAGE. 1998. Genetic variation and phylogeography of central Asian and other house mice, including a major new mitochondrial lineage in Yemen. Genetics, 150: 835-861.
64. RODRIGUEZ, R. M., and L. K. AMMERMAN. 2004. Mitochondrial DNA divergence does not reflect morphological difference between Myotis californicus and Myotis ciliolabrum. Journal of Mammalogy, 85: 842-851.
65. RUEDI, M., and V. CASTELLA. 2003. Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: a mitochon -drial and nuclear survey. Molecular Ecology, 12: 1527-1540.
66. RUEDI, M., and F. MAYER. 2001. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Molecular Phylogenet -ics and Evolution, 21: 436-448.
67. RUEDI, M., S. WALTER, M. C. FISHER, D. SCARAVELLI, L. EXCOF -FIER and G. HECKEL. 2008. Italy as a major Ice Age refugee area for the bat Myotis myotis (Chiroptera: Vespertilionidae) in Europe. Molecular Ecology, 17: 1801-1814.
68. RUSSO, D., G. JONES, and R. ARLETTAZ. 2007. Echolocation and passive listening by foraging mouse-eared bats Myotis myotis and M. blythii. Journal of Experimental Biology, 210: 166-176.
69. SEDDON, J. M., F. SANTUCCI, N. J. REEVE, and G. M. HEWITT. 2002. Caucasus Mountains divide postulated postglacial col -o nization routes in the white-breasted hedgehog, Erina ceus concolor. Journal of Evolutionary Biology, 15: 463-467.
70. SEVILLA, P. 1989. Quaternary fauna of bats in Spain: paleoecologic and biogeographic interest. Pp. 349-355, in European bat research 1987 (V. HANAK, I. HORA?EK, and J. GAISLER, eds.). Charles University Press, Praha, 718 pp.
71. SHAPIRO, B., A. J. DRUMMOND, A. RAMBAUT, M. C. WILSON, P. E. MATHEUS, A.V. SHER, O. G. PYBUS, et al. 2004. Rise and fall of the Beringian steppe bison. Science, 306: 1561-1565.
72. SIMMONS, N. B. 2005. Order Chiroptera. Pp. 312-529, in Mammal species of the World: a taxonomic and geographical reference, 3rd edition (D. E. WILSON and D. M. REEDER, eds.). Johns Hopkins University Press, Baltimore, 2142 pp.
73. SOLARI, S., S. R. HOOFER, P. A. LARSEN, A. D. BROWN, R. J. BULL, J. A. GUERRERO, J. ORTEGA, J. P. CARRERA, R. D. BRADLEY, and R. J. BAKER. 2009. Operational criteria for genetically defined species: analysis of the diversification of the small fruit-eating bats, Dermanura (Phyllostomidae: Stenodermatinae). Acta Chiropterologica, 11: 279-288.
74. SOMMER, R. S., and A. NADACHOWSKI. 2006. Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Review, 36: 251-265.
75. STRELKOV, P. P. 1972. Myotis blythi (Tomes, 1857): distrib u tion, geographical, variability and differences from Myotis myotis (Borkhausen, 1797). Acta Theriologica, 28: 355-380.
76. SWOFFORD, D. L. 2000. PAUP*. Phylogenetic analysis using par simony (*and other methods). Version 4. Sinauer Asso -ciates, Sunderland, MA.
77. SZTENCEL-JABONKA, A., G. JONES, and W. BOGDANOWICZ. 2009. Skull morphology of two cryptic bat species: Pipi -strellus pipistrellus and P. pygmaeus ? a 3D geometric mor phometrics approach with landmark reconstruction. Acta Chiropterologica, 11: 113-126.
78. TABERLET, P., and R. CHEDDADI. 2002. Quaternary refugia and persistence of biodiversity. Science, 297: 2009-2010.
79. TEELING, E. C., M. SCALLY, D. J. KAO, M. L. ROMAGNOLI, M. S. SPRINGER, and M. J. STANHOPE. 2000. Molecular evidence regarding the origin of echolocation and flight in bats. Nature, 403: 188-192.
80. THOMPSON, J. D., T. J. GIBSON, F. PLEWNIAK, F. JEANMOUGIN, and D. G. HIGGINS. 1997. The ClustalX windows interface: flex ible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25: 4876-4882.
81. TOPAL, G., and M. RUEDI. 2001. Myotis blythii (Tomes, 1857) - Kleines Mausohr. Pp. 209-255, in Handbuch der Saugetiere Europas. Band 4: Fledertiere. Teil I: Chiroptera I. Rhinolo phidae, Vespertilionidae 1 (F. KRAPP, ed.). Aula-Verlag, Wiebels heim, 603 pp.
82. WEAVER, K. N., S. E. ALFANO, A. R. KRONQUIST, and D. M. REEDER. 2009. Healing rates of wing punch wounds in freeranging little brown myotis (Myotis lucifugus). Acta Chiropterologica, 11: 220-223.
83. WETTSTEIN, P. J., M. STRAUSBAUCH, T. LAMB, J. STATES, R. CHAKRABORTY, L. JIN, and R. RIBLET. 1995. Phylogeny of six Sciurus aberti subspecies based on nucleotide sequences of cytochrome b.Molecular Phylogenetics and Evolution, 4: 150-162.
84. WORTHINGTON WILMER, J., and E. BARRATT. 1996. A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Research News, 37: 1-3.
85. ZAHN, A. 1999. Reproductive success, colony size and roost temperature in attic-dwelling bat Myotis myotis. Journal of Zoology (London), 247: 275-280.
86. ZAHN, A., L. RODRIGUES, A. RAINHO, and J. M. PALMEIRIM. 2007. Critical times of the year for Myotis myotis, a temperate zone bat: roles of climate and food resources. Acta Chiropterologica, 9: 115-125.