Population genetics study of common (Pipistrellus pipistrellus) and soprano (Pipistrellus pygmaeus) pipistrelle bats from central Europe suggests interspecific hybridization

Canadian Journal of Zoology

Volumn 90, Issue 10, 2012, Pages 1251-1260

  Sztencel Jablonka A ^a   Bogdanowicz, W ^a  

^a MUSEUM AND INSTITUTE OF ZOOLOGY   (Poland)

Author keywords

Common pipistrelle; Genetic structure; Hybridization; Hybrids; Microsatellites; Pipistrellus pipistrellus; Pipistrellus pygmaeus; Population genetics; Soprano pipistrelle

Indexed keywords

BAT; BAYESIAN ANALYSIS; COEXISTENCE; COLONY STRUCTURE; CRYPSIS; GENETIC VARIATION; HYBRIDIZATION; INTERSPECIFIC INTERACTION; MIGRATORY BEHAVIOR; POPULATION GENETICS;

EUROPE;

PIPISTRELLUS; PIPISTRELLUS PIPISTRELLUS; PIPISTRELLUS PYGMAEUS;

EID: 84871706186     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/Z2012-092     Document Type: Article

References (73)

1. Ahlén, I. 1981. Identification of Scandinavian bats by their sounds. Swedish University of Agricultural Science Report No. 6. pp. 1-56.
2. Anděra, M., and Hanák, V. 2007. Atlas of mammals of the Czech Republic-a provisional version. V. Bats (Chiroptera)-Part 3. Vespertilionid bats (Vespertilionidae-Vespertilio, Eptesicus, Nyctalus, Pipistrellus and Hypsugo). National Museum, Prague.
3. Anderson, E.C. 2002. User's guide to the program NewHybrids. Version 1.0 [computer program]. Available from http://ib.berkeley.edu/labs/slatkin/eriq/software/new_hybs_doc.pdf [accessed 20 November 2011].
4. Anderson, E.C., and Thompson, E.A. 2002. A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160(3): 1217-1229. PMID:11901135.
5. Artyushin, I.V., Bannikova, A.A., Lebedev, V.S., and Kruskop, S.V. 2009. Mitochondrial DNA relationships among North Palaearctic Eptesicus (Vespertilionidae, Chiroptera) and past hybridization between common serotine and northern bat. Zootaxa, 2262: 40-52.
6. Avery, M.I. 1991. Pipistrelle. In Handbook of British mammals. Edited by G.B. Corbet and S. Harris. Blackwell Publications, Oxford. pp.124-128.
7. Bachanek, J., and Postawa, T. 2010. Morphological evidence for hybridization in the sister species Myotis myotis and Myotis oxygnathus (Chiroptera: Vespertilionidae) in the Carpathian Basin. Acta Chiropt. 12(2): 439-448. doi:10.3161/150811010X538007.
8. Barlow, K.E. 1997. The diets of two phonic types of the bat Pipistrellus pipistrellus in Britain. J. Zool. (Lond.), 243(3): 597-609. doi:10.1111/j.1469-7998.1997.tb02804.x.
9. Barratt, E.M., Deaville, R., Burland, T.M., Bruford, M.W., Jones, G., Racey, P.A., and Wayne, R.K. 1997. DNA answers the call of pipistrelle bat species. Nature, 387(6629): 138-139. doi:10.1038/ 387138b0. PMID:9144281.
10. Benjamini, Y., and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57(1): 289-300.
11. Berthier, P., Excoffier, L., and Ruedi, M. 2006. Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc. R. Soc. Lond. B Biol. Sci. 273(1605): 3101-3123. doi:10.1098/rspb.2006.3680. PMID:17018432.
12. Bogdanowicz, W., Van Den Bussche, R., Gajewska, M., Postawa, T., and Harutyunyan, M. 2009. Ancient and contemporary DNA sheds light on the history of mouse-eared bats in Europe and the Caucasus. Acta Chiropt. 11(2): 289-305. doi:10.3161/ 150811009X485530.
13. Brookfield, J.F.Y. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5(3): 453-455. doi:10.1046/j.1365-294X.1996.00098.x. PMID: 8688964.
14. Bryja, J., Kaňuch, P., Fornůsková, A., Bartonička, T., and Řehák, Z. 2009. Low population genetic structuring of two cryptic bat species suggests their migratory behaviour in continental Europe. Biol. J. Linn. Soc. 96(1): 103-114. doi:10.1111/j.1095-8312.2008. 01093.x.
15. Burgarella, C., Lorenzo, Z., Jabbour-Zahab, R., Lumaret, R., Guichoux, E., Petit, R.J., Soto, Á., and Gil, L. 2009. Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity, 102(5): 442-452. doi:10.1038/hdy.2009.8. PMID: 19240752.
16. Chapuis, M.P., and Estoup, A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24(3): 621-631. doi:10.1093/molbev/msl191. PMID:17150975.
17. Cornuet, J.M., and Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144(4): 2001-2014. PMID:8978083.
18. Davidson-Watts, I., Walls, S., and Jones, G. 2006. Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats. Biol. Conserv. 133(1): 118-127. doi:10.1016/ j.biocon.2006.05.027.
19. Dietz, D., and von Helversen, O. 2004. Illustrated identification key to the bats of Europe. Version 1.0. Available from http://biocenosi.dipbsf.uninsubria.it/didattica/bat_key1.pdf [accessed 20 November 2011].
20. Dietz, D., von Helversen, O., and Nill, D. 2009. Bats of Britain, Europe and Northwest Africa. A&C Black, London.
21. Durrant, C.J., Beebee, T.J.C., Greenaway, F., and Hill, D.A. 2009. Evidence of recent population bottlenecks and inbreeding in British populations of Bechstein's bat, Myotis bechsteinii. Conserv. Genet. 10(2): 489-496. doi:10.1007/s10592-008-9639-5.
22. Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611-2620. doi:10.1111/j. 1365-294X.2005.02553.x. PMID:15969739.
23. Excoffier, L., and Lischer, H.E.L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10(3): 564-567. doi:10. 1111/j.1755-0998.2010.02847.x. PMID:21565059.
24. Fitzpatrick, B.M. 2004. Rates of evolution of hybrid inviability in birds and mammals. Evolution, 58(8): 1865-1870. doi:10.1554/04-190. PMID:15446440.
25. Fornůsková, A. 2009. Population genetic structure of two cryptic species of the genus Pipistrellus in Central Europe. Research Master 2 thesis, Masaryk University, Brno. Available from http://is.muni.cz/th/143906/prif_m/Thesis_Fornuskova_2009.pdf [ac-cessed 20 November 2011].
26. Goodnight, K.F., and Queller, D.C. 2004. Relatedness 5.0 manual. Available from http://www.gsoftnet.us/GSoft.html [accessed 20 January 2011].
27. Goudet, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86(6): 485-486.
28. Goudet, J. 2001. Fstat, a program to estimate and test gene diversities and fixation indices. Version 2.9.3 [computer program]. Available from http://www2.unil.ch/popgen/softwares/fstat.htm [accessed 20 November 2011].
29. Goudet, J., Raymond, M., de Meeüs, T., and Rousset, F. 1996. Testing differentiation in diploid population. Genetics, 144(4): 1933-1940. PMID:8978076.
30. Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
31. Hulva, P., Horáček, I., Strelkov, P.P., and Benda, P. 2004. Molecular architecture of Pipistrellus pipistrellus/Pipistrellus pygmaeus complex (Chiroptera: Vespertilionidae): further cryptic species and Mediterranean origin of the divergence. Mol. Phylogenet. Evol. 32(3): 1023-1035. doi:10.1016/j.ympev.2004.04.007. PMID:15288073.
32. Hulva, P., Fornůsková, A., Chudárková, A., Evin, A., Allegrini, B., Benda, P., and Bryja, J. 2010. Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Mol. Ecol. 19(24): 5417-5431. doi:10.1111/j.1365-294X.2010.04899.x. PMID:21054608.
33. Hutson, A.M., Spitzenberger, F., Aulagnier, S., Coroiu, I., Karataş, A., Juste, J., Paunovic, M., Palmeirim, J., and Benda, P. 2008a. Pipistrellus pipistrellus. In IUCN 2011 red list of threatened species. Version 2011.2. Available from www.iucnredlist.org [accessed 10 April 2012].
34. Hutson, A.M., Spitzenberger, F., Aulagnier, S., Coroiu, I., Karataş, A., Juste, J., Paunovic, M., Palmeirim, J., and Benda, P. 2008b. Pipistrellus pygmaeus. In IUCN 2011. IUCN red list of threatened species. Version 2011.2. Available from www.iucnredlist.org [accessed 10 April 2012].
35. Hutterer, R., Ivanova, T., Meyer-Cords, C., and Rodrigues, L. 2005. Bat migrations in Europe: a review of banding data and literature. Federal Agency for Nature Conservation, Bonn, Germany. Available from http://www.gbv.de/dms/bs/toc/509921078.pdf [accessed 20 November 2011]
36. Ibáñez, C., Garcia-Mudarra, J.L., Ruedi, M., Stadelmann, B., and Juste, J. 2006. The Iberian contribution to cryptic diversity in European bats. Acta Chiropt. 8(2): 277-297. doi:10.3161/1733-5329(2006)8[277:TICTCD]2.0.CO;2.
37. Jadwiszczak, P. 2009. Rundom Pro 3.14. Software for classical and computer-intensive statistics. Available from http://pjadw.tripod.com [accessed 10 January 2011].
38. Jones, G., and Barratt, E.M. 1999. Vespertilio pipistrellus Schreber, 1774 and V. pygmaeus Leach, 1825 (currently Pipistrellus pipistrellus and P. pygmaeus; Mammalia, Chiroptera): proposed designation of neotypes. Bull. Zool. Nomencl. 56: 182-186. Available from http://biostor.org/reference/2783 [accessed 20 December 2010.]
39. Jones, G., and van Parijs, S.M. 1993. Bimodal echolocation in pipistrelle bats: are cryptic species present? Proc. R. Soc. Lond. B Biol. Sci. 251(1331): 119-125. doi:10.1098/rspb.1993.0017. PMID:8096079.
40. Kaňuch, P., Hájková, P., Řehák, Z., and Bryja, J. 2007. A rapid PCR-based test for species identification of two cryptic bats Pipistrellus pipistrellus and P. pygmaeus and its application on museum and dropping samples. Acta Chiropt. 9(1): 277-282. doi:10.3161/ 1733-5329(2007)9[277:ARPTFS]2.0.CO;2.
41. Kaňuch, P., Fornůsková, A., Bartonička, T., Bryja, J., and Řehák, Z. 2010. Do two cryptic pipistrelle bat species differ in their autumn and winter roosting strategies within the range of sympatry? Folia Zool. (Brno), 59: 102-107.
42. Larsen, P.A., Marchan-Rivadeneira, M.R., and Baker, R.J. 2010. Natural hybridization generates mammalian lineage with species characteristics. Proc. Natl. Acad. Sci. U.S.A. 107(25): 11447-11452. doi:10.1073/pnas.1000133107. PMID:20534512.
43. Mallet, J. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20(5): 229-237. doi:10.1016/j.tree.2005.02.010. PMID:16701374.
44. Mallet, J. 2008. Hybridization, ecological races, and the nature of species: empirical evidence for the ease of speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363(1506): 2971-2986. doi:10. 1098/rstb.2008.0081. PMID:18579473.
45. Mao, X., Zhang, J., Zhang, S., and Rossiter, S.J. 2010. Historical male-mediated introgression in horseshoe bats revealed by multilocus DNA sequence data. Mol. Ecol. 19(7): 1352-1366. doi:10. 1111/j.1365-294X.2010.04560.x. PMID:20298473.
46. Miller-Butterworth, C.M., Jacobs, D.S., and Harley, E.H. 2003. Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature, 424(6945): 187-191. doi:10. 1038/nature01742. PMID:12853955.
47. Nagy, Z.L., and Szántó, L. 2003. The occurrence of hibernating Pipistrellus pipistrellus (Schreber, 1774) in caves of the Carpathian Basin. Acta Chiropt. 5: 155-160.
48. Nicholls, B., and Racey, P.A. 2006. Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus. Ecography, 29(5): 697-708. doi:10.1111/j.2006.0906-7590.04575.x.
49. Paetkau, D., Slade, R., Burden, M., and Estoup, A. 2004. Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol. Ecol. 13(1): 55-65. doi:10.1046/j.1365-294X.2004. 02008.x. PMID:14653788.
50. Park, K.J., Altringham, J.D., and Jones, G. 1996. Assortative roosting in the two phonic types of Pipistrellus pipistrellus during the mating season. Proc. R. Soc. Lond. B Biol. Sci. 263(1376): 1495-1499. doi:10.1098/rspb.1996.0218.
51. Peakall, R., and Smouse, P.E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes, 6(1): 288-295. doi:10.1111/j.1471-8286.2005.01155.x.
52. Piry, S., Alapetite, A., Cornuet, J.M., Paetkau, D., Baudouin, L., and Estoup, A. 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95(6): 536-539. doi:10.1093/jhered/esh074. PMID:15475402.
53. Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2): 945-959. PMID:10835412.
54. Queller, D.C., and Goodnight, K.F. 1989. Estimating relatedness using genetic markers. Evolution, 43(2): 258-275. doi:10.2307/2409206.
55. Racey, P.A., Barratt, E.M., Burland, T.M., Deaville, R., Gotelli, D., Jones, G., and Piertney, S.B. 2007. Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species. Biol. J. Linn. Soc. 90(3): 539-550. doi:10.1111/j.1095-8312.2007. 00746.x.
56. Raymond, M., and Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
57. Rousset, F. 2008. GENEPOP'007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8(1): 103-106. doi:10.1111/j.1471-8286.2007.01931.x. PMID: 21585727.
58. Sachanowicz, K., and Ciechanowski, M. 2005. Nietoperze Polski [Bats of Poland]. Multico Oficyna Wydawnicza, Warszawa.
59. Sanz, N., Araguas, R.M., Fernández, R., Vera, M., and García-Marín, J.-L. 2009. Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conserv. Genet. 10(1): 225-236. doi:10.1007/s10592-008-9550-0.
60. Stadelmann, B., Herrera, L.G., Arroyo-Cabrales, J., Flores-Martínez, J.J., May, B.P., and Ruedi, M. 2004. Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. J. Mammal. 85(1): 133-139. doi:10.1644/1545-1542(2004)085<0133:MSOTFB>2.0.CO;2.
61. StatSoft Inc. 2005. STATISTICA (data analysis software system). Version 7.1 [computer program]. StatSoft Inc., Tulsa, Okla. Available from www.statsoft.com [accessed 15 January 2011].
62. Storey, J.D. 2002. A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B Stat. Methodol. 64(3): 479-498. doi:10.1111/ 1467-9868.00346.
63. Sztencel-Jablonka, A., Jones, G., and Bogdanowicz, W. 2009. Skull morphology of two cryptic bat species: Pipistrellus pipistrellus and P. pygmaeus-a 3D geometric morphometrics approach with landmark reconstruction. Acta Chiropt. 11(1): 113-126. doi:10. 3161/150811009X465730.
64. Thompson, M.J.A. 1992. Roost philopatry in female pipistrelle bats Pipistrellus pipistrellus. J. Zool. (Lond.), 228(4): 673-679. doi:10.1111/j.1469-7998.1992.tb04466.x.
65. Vähä, J.P., and Primmer, C.R. 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 15(1): 63-72. doi:10.1111/j.1365-294X.2005.02773.x. PMID:16367830.
66. van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., and Shipley, P.F. 2003. Micro-checker version 2.2.3. Department of Biological Sciences and Department of Computer Science, University of Hull, Hull, UK. Available from http://www.microchecker.hull.ac.uk [accessed 20 January 2011].
67. Vaughan, N., Jones, G., and Harris, S. 1997. Habitat use by bats (Chiroptera) assessed by means of a broad-brand acoustic method. J. Appl. Ecol. 34(3): 716-730. doi:10.2307/2404918.
68. Vonhof, M.J., Davis, C.S., Fenton, M.B., and Strobeck, C. 2002. Characterization of dinucleotide microsatellite loci in big brown bats (Eptesicus fuscus), and their use in other North American vespertilionid bats. Mol. Ecol. Notes, 2(2): 167-169. doi:10.1046/ j.1471-8286.2002.00189.x.
69. Webb, N.J., and Tidemann, C.R. 1995. Hybridisation between black (Pteropus alecto) and grey-headed (P. poliocephalus) flying-foxes (Megachiroptera: Pteropodidae). Aust. Mammal. 18: 19-26.
70. Weid, R., and von Helversen, O. 1987. Ortungsrufe europäischer Fledermäuse beim Jagdflug im Freiland. Myotis, 25: 5-27.
71. Wicht, B., Moretti, M., Preatoni, D., Tosi, G., and Martinoli, A. 2003. The presence of soprano pipistrelle Pipistrellus pygmaeus (Leach, 1825) in Switzerland: first molecular and bioacoustic evidences. Rev. Suisse Zool. 110: 411-426.
72. Worthington-Wilmer, J., and Barratt, E.M. 1996. A non-lethal method of tissue sampling for genetic studies of microchiropterans. Bat. Res. News, 37: 1-3.
73. Zingg, P. 1990. Akustische Artidentifikation von Fledermäusen (Mammalia: Chiroptera) in der Schweiz. Rev. Suisse Zool. 97: 263-294.