Low population genetic structuring of two cryptic bat species suggests their migratory behaviour in continental Europe

Biological Journal of the Linnean Society

Volumn 96, Issue 1, 2009, Pages 103-114

  Bryja, Josef ^a,b   Kaňuch, Peter ^a,c   Fornůsková, Alena ^a,b   Bartonička, Tomáš ^b   Řehák, Zdeněk ^b  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^b MASARYK UNIVERSITY   (Czech Republic)

^c INSTITUTE OF FOREST ECOLOGY   (Slovakia)

Author keywords

Colony structure; Dispersal; Gene flow; Microsatellites; Relatedness

Indexed keywords

BAT; COLONY STRUCTURE; CRYPSIS; DISPERSAL; GENETIC STRUCTURE; HIBERNATION; MIGRATORY BEHAVIOR; POPULATION GENETICS; RELATEDNESS;

EURASIA; EUROPE;

PIPISTRELLUS PIPISTRELLUS; PIPISTRELLUS PYGMAEUS; VESPERTILIONIDAE;

EID: 58149100118     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2008.01093.x     Document Type: Article

References (91)

1. Ahlén I. 1981. Identification of Scandinavian bats by their sounds. Swedish University of Agricultural Sciences, Rapport 6 : 1 56.
2. Ahlén I. 1997. Migratory behaviour of bats at south Swedish coasts. Zeitschrift Für Saugetierkunde 62 : 375 380.
3. Anděra M, Hanák V. 2007. Atlas of the mammals of the Czech Republic - a provisional version. V. Bats (chiroptera) - part 3. Prague : National Museum.
4. Avery MI. 1991. Pipistrelle. In : Corbet GB, Harris S, eds. Handbook of British mammals. Oxford : Blackwell Scientific Publications, 124 128.
5. Barlow KE, Jones G. 1999. Roosts, echolocation calls and wing morphology of two phonic types of Pipistrellus pipistrellus. Zeitschrift für Säugetierkunde 64 : 257 268.
6. Barratt EM, Bruford MW, Burland TM, Jones G, Racey PA, Wayne RK. 1995. Characterization of mitochondrial DNA variability within the microchiropteran genus Pipistrellus: approaches and applications. Symposia of the Zoological Society of London 67 : 377 386.
7. Barratt EM, Deaville R, Burland TM, Bruford MW, Jones G, Racey PA, Wayne RK. 1997. DNA answers the call of pipistrelle bat species. Nature 387 : 138 139.
8. Bartonička T, Řehák Z. 2004. Flight activity and habitat use of Pipistrellus pygmaeus in a floodplain forest. Mammalia 68 : 365 375.
9. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. 2001. GENETIX 4.02, Logiciel sous windows TM pour la Génétique des Populations. Montpellier : Laboratoire Génome, Populations, Interactions, Université de Montpellier II.
10. Belkhir K, Castric V, Bonhomme F. 2002. IDENTIX, a software to test for relatedness in a population using permutation methods. Molecular Ecology Notes 2 : 611 614.
11. Benda P, Ivanova T, Horáček I, Hanák V, Červený J, Gaisler J, Gueorguieva A, Petrov B, Vohralík V. 2003. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 3. Review of bat distribution in Bulgaria. Acta Societatis Zoologicae Bohemicae 67 : 245 357.
12. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B, Statistical Methology 57 : 289 300.
13. Brouat C, Loiseau A, Kane A, Ba K, Duplantier JM. 2007. Population genetic structure of two ecologically distinct multimammate rats: the commensal Mastomys natalensis and the wild Mastomys erythroleucus in southeastern Senegal. Molecular Ecology 16 : 2985 2997.
14. Buerkle CA. 1999. The historical pattern of gene flow among migratory and nonmigratory populations of prairie warblers (Aves: Parulinae). Evolution 53 : 1915 1924.
15. Burland TM, Barrat EM, Beaumont MA, Racey PA. 1999. Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proceedings of the Royal Society of London Series B, Biological Sciences 266 : 975 980.
16. Burland TM, Worthington-Wilmer J. 2001. Seeing in the dark: molecular approaches to the study of bat populations. Biological Reviews 76 : 389 409.
17. Castella V, Ruedi M, Excoffier L. 2001. Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. Journal of Evolutionary Biology 14 : 708 720.
18. Castella V, Ruedi M, Excoffier L, Ibánez C, Arlettaz R, Hausser J. 2000. Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Molecular Ecology 9 : 1761 1772.
19. Chapuis MP, Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24 : 621 631.
20. Cockrum EL. 1969. Migration in guano bat, Tadarida brasiliensis. Miscellaneos Publicaion, University of Kansas, Museum of Natural History 51 : 303 336.
21. Davidson-Watts I, Jones G. 2006. Differences in foraging behaviour between Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus pygmaeus (Leach, 1825). Journal of Zoology, London 268 : 55 62.
22. Davidson-Watts I, Walls S, Jones G. 2006. Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats. Biological Conservation 133 : 118 127.
23. Davis LA, Roalson EH, Cornell KL, McClanahan KD, Webster MS. 2006. Genetic divergence and migration patterns in a North American passerine bird: implications for evolution and conservation. Molecular Ecology 15 : 2141 2152.
24. Dumitru M. 1995. Mammal species from Romania categories of conservation. Travaux du Museum National d'Histoire Naturelle Grigore Antipa 35 : 549 566.
25. 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.
26. Falush D, Stephens M, Pritchard JK. 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7 : 574 578.
27. Feyerabend F, Simon M. 2000. Use of roosts and roost switching in a summer colony of 45 kHz phonic type pipistrelle bats Pipistrellus pipistrellus Schreber, 1774. Myotis, Bonn 38 : 51 59.
28. Furmankiewicz J, Altringham J. 2007. Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites. Conservation Genetics 8 : 913 923.
29. Gaisler J, Hanák V, Hanzal V, Jarský V. 2003. Results of bat banding in the Czech Republic and Slovakia, 1948-2000. Vespertilio 7 : 3 61.
30. Gaisler J, Řehák Z, Bartonička T. 2002. Mammalia: chiroptera. In : Řehák Z, Gaisler J, Chytil J, eds. Vertebrates of the Pálava Biosphere Reserve of UNESCO. Brno : Masaryk University, 139 149.
31. Gaisler J, Zukal J, Řehák Z, Homolka M. 1998. Habitat preference and flight activity of bats in a city. Journal of Zoology, London 244 : 439 445.
32. Gerell R, Lundberg K. 1985. Social organization in the bat Pipistrellus pipistrellus. Behavioral Ecology and Sociobiology 16 : 177 184.
33. Goudet J. 2001. FSTAT: a program to estimate and test gene diversities and fixation indices, Version 2.9.3. Available at: http://www.unil.ch/izea/ softwares/fstat.html
34. Goudet J, Raymond M, deMeeus T, Rousset F. 1996. Testing differentiation in diploid populations. Genetics 144 : 1933 1940.
35. Hedrick PW. 2005. A standardized genetic differentiation measure. Evolution 59 : 1633 1638.
36. Hellgren O, Bensch S, Hobson KA, Lindström A. 2008. Population structure and migratory directions of Scandinavian bluethroats Luscinia svecica- a molecular, morphological and stable isotope analysis. Ecography 31 : 95 103.
37. von Helversen O, Esche M, Kretzschmar F, Boschert M. 1987. Die Fledermäuse Südbadens. Mitteilungen des badischen Landesvereins für Naturkunde und Naturschutz NF 14 : 409 475.
38. Hutterer R, Ivanova T, Meyer-Cords Ch, Rodrigues L. 2005. Bat migrations in Europe. A review of banding data and literature. Bonn : Federal Agency for Nature Conservation.
39. Höglund J, Alatalo RV. 1995. Leks. Princeton, NJ : Princeton University Press.
40. Jones G. 1999. Pipistrellus pipistrellus (Schreber, 1774). In : Mitchell-Jones AJ, Amori G, Bogdanowicz W, Kryštufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralík V, Zima J, eds. The atlas of european mammals. London : Academic Press, 126 127.
41. Kalinowski ST, Wagner AP, Taper ML. 2006. ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6 : 576 579.
42. Kaňuch P, Fornůsková A, Bartonička T, Bryja J. 2007a. Multiplex panels of polymorphic microsatellite loci for two cryptic bat species of the genus Pipistrellus, developed by cross-species amplification within the family Vespertilionidae. Molecular Ecology Notes 7 : 871 873.
43. Kaňuch P, Hájková P, Řehák Z, Bryja J. 2007b. 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 Chiropterologica 9 : 277 282.
44. Kepka O. 1981. Fledermäuse der Steiermark. Myotis, Bonn 18 19 : 168 179.
45. Kerth G, Mayer F, Petit E. 2002a. Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein's bat (Myotis bechsteinii). Molecular Ecology 11 : 1491 1498.
46. Kerth G, Safi K, König B. 2002b. Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii). Behavioral Ecology and Sociobiology 52 : 203 210.
47. Kerth G, Petit E. 2005. Colonization and dispersal in a social species, the Bechstein's bat (Myotis bechsteinii). Molecular Ecology 14 : 3943 3950.
48. Kretzschmar F, Heinz B. 1995. Social behaviour and hibernation of a large population of Pipistrellus pipistrellus (Schreber, 1774) (Chiroptera: Vespertilionidae) and some other bat species in the mining-system of a limestone quarry near Heidelberg (South West Germany). Myotis, Bonn 32 33 : 221 231.
49. Lundberg K, Gerell R. 1986. Territorial advertisement and mate attraction in the bat Pipistrellus pipistrellus. Ethology 71 : 115 124.
50. Matis Š, Uhrin M, Pjenčák P. 2002. Hibernation of bats in Erna cave. Vespertilio 6 : 235 236.
51. McCracken GF, Lumsden LF, Kunz TH. 2006. Roosting ecology and population biology. In : Zubaid A, McCracken GF, Kunz TH, eds. Functional and evolutionary ecology of bats. New York, NY : Oxford University Press, 179 184.
52. McCracken GF, McCracken MK, Vawter AT. 1994. Genetic structure in migratory populations of the bat Tadarida brasiliensis mexicana. Journal of Mammalogy 75 : 500 514.
53. Meirmans PG. 2006. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60 : 2399 2402.
54. Nagy ZL, Szanto L. 2003. The occurrence of hibernating Pipistrellus pipistrellus (Schreber, 1774) in caves of The Carpathian Basin. Acta Chiropterologica 5 : 155 160.
55. Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 : 583 590.
56. Nicholls B, Racey PA. 2006a. Contrasting home-range size and spatial partitioning in cryptic and sympatric pipistrelle bats. Behavioral Ecology and Sociobiology 61 : 131 142.
57. Nicholls B, Racey PA. 2006b. Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus. Ecography 29 : 697 708.
58. Norberg UM, Rayner JM. 1987. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptions, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London Series B 316 : 335 427.
59. Park KJ, Altringham JD, Jones G. 1996. Assortative roosting in the two phonic types of Pipistrellus pipistrellus during the mating season. Proceedings of the Royal Society of London Series B, Biological Sciences 263 : 1495 1499.
60. Peakall R, Smouse PE. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6 : 288 295.
61. Petit E, Balloux F, Goudet J. 2001. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55 : 635 640.
62. Petit E, Mayer F. 1999. Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proceedings of the Royal Society of London Series B, Biological Sciences 266 : 1717 1722.
63. Petit E, Mayer F. 2000. A population genetic analysis of migration: the case of the noctule bat (Nyctalus noctula). Molecular Ecology 9 : 683 690.
64. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155 : 945 959.
65. Queller DC, Goodnight KF. 1989. Estimating relatedness using genetic markers. Evolution 43 : 258 275.
66. Racey PA, Barratt EM, Burland TM, Deaville R, Gotelli D, Jones G, Piertney SB. 2007. Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species. Biological Journal of the Linnean Society 90 : 539 550.
67. Rachwald A. 1992. Social organization, recovery frequency and body weight of the bat Pipistrellus nathusii from northern Poland. Myotis, Bonn 30 : 109 118.
68. Raymond M, Rousset F. 1995. GENEPOP (version 1.2): population genetic software for exact tests and eucumenism. Journal of Heredity 86 : 248 249.
69. Rivers NM, Butlin RK, Altringham JD. 2005. Genetic population structure of Natterer's bats explained by mating at swarming sites and philopatry. Molecular Ecology 14 : 4299 4312.
70. Rodrigues L, Palmeirim JM. 2008. Migratory behaviour of the Schreiber's bat: when, where and why do cave bats migrate in a Mediterranean region? Journal of Zoology, London 274 : 116 125.
71. Roer H. 1989. Field experiments about the homming behaviour of the common pipistrelle (Pipistrellus pipistrellus, Schreber). In : Hanák V, Horáček I, Gaisler J, eds. European bat research 1987. Prague : Charles University Press, 551 558.
72. Rossiter SJ, Benda P, Dietz C, Zhang S, Jones G. 2007. Rangewide phylogeography in the greater horsehoe bat inferred from microsatellites: implications for population history, taxonomy and conservation. Molecular Ecology 16 : 4699 4714.
73. Rossiter SJ, Jones G, Ransome RD, Barratt EM. 2000. Genetic variation and population structure in the endangered greater horsehoe bat Rhinolophus ferrumequinum. Molecular Ecology 9 : 1131 1135.
74. Rousset F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation-by distance. Genetics 145 : 1219 1228.
75. Ruczyński I, Bogdanowicz W. 2005. Roost cavity selection by Nyctalus noctula and N. leisleri (Vespertilionidae, Chiroptera) in Bialowieza Primeval Forest, Eastern Poland. Journal of Mammalogy 86 : 921 930.
76. Russ JM, Hutson AM, Montgomery WI, Racey PA, Speakman JR. 2000. The status of Nathusius pipistrelle (Pipistrellus nathusii Keyserling et Blasius, 1839) in the British Isles. Journal of Zoology, London 254 : 91 100.
77. Russell AL, Medellín RA, McCracken GF. 2005. Genetic variation and migration in the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Molecular Ecology 14 : 2207 2222.
78. Rydell J, Baagøe HJ. 1994. Vespertilio murinus. Mammalian Species 467 : 1 6.
79. Sachteleben J. 1991. Zum 'Invasions' - Verhalten der Zwergfledermaus (Pipistrellus pipistrellus). Nyctalus (NF) 4 : 51 66.
80. Sachteleben J, von Helversen O. 2006. Songflight behaviour and mating system of pipistrelle bat (Pipistrellus pipistrellus) in an urban habitat. Acta Chiropterologica 8 : 391 401.
81. Sattler T, Bontadina F, Hirzel AH, Arlettaz R. 2007. Ecological niche modelling of two cryptic bat species calls for a reassessment of their conservation status. Journal of Applied Ecology 44 : 1188 1199.
82. Sendor T, Kugelschafter K, Simon M. 2000. Seasonal variation of activity patterns at a pipistrelle (Pipistrellus pipistrellus) hibernaculum. Myotis, Bonn 38 : 91 109.
83. Sendor T, Simon M. 2003. Population dynamics of the pipistrelle bat: effects of sex, age and winter weather on seasonal survival. Journal of Animal Ecology 72 : 308 320.
84. Shiel CB, Fairley JS. 1999. Evening emergence of two nursery colonies of Leisler's bat (Nyctalus leisleri). Ireland. Journal of Zoology, London 247 : 439 447.
85. Smit-Viergutz J, Simon M. 2000. Eine vergleichende Analyse des sommerrlichen Schwärmverhaltens der Zwergfledermaus (45 kHz Ruftyp, Pipistrellus pipistrellus Schreber, 1774) an den Invasionsorten und am Winterquartier. Myotis, Bonn 38 : 69 89.
86. Storey JD. 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society Series B, Statistical Methology 64 : 479 498.
87. Strelkov PP. 1969. Migratory and stationary bats (Chiroptera) of the European part of the Soviet Union. Acta Zoologica, Cracow 14 : 393 440.
88. Wagner AP, Creel S, Kalinowski ST. 2006. Estimating relatedness and relationships using microsatellite loci with null alleles. Heredity 97 : 336 345.
89. Webb NJ, Tidemann CR. 1996. Mobility of Australian flying-foxes, Pteropus spp. (Megachiroptera): evidence from genetic variation. Proceedings of the Royal Society of London Series B, Biological Sciences 263 : 497 502.
90. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38 : 1358 1370.
91. Zingg P. 1990. Akustische Artidentifikation von Fledermäusen (Mammalia: Chiroptera) in der Schweiz. Revue suisse Zoologie 97 : 263 294.