Conservation Genetics

, Volume 19, Issue 2, pp 481–494 | Cite as

Comparative phylogeography of a vulnerable bat and its ectoparasite reveals dispersal of a non-mobile parasite among distinct evolutionarily significant units of the host

  • J. van Schaik
  • D. Dekeukeleire
  • S. Gazaryan
  • I. Natradze
  • G. Kerth
Research Article


Knowledge about phylogeographical structuring and genetic diversity is of key importance for the conservation of endangered species. Comparative phylogeography of a host and its parasite has the potential to reveal cryptic dispersal and behaviour in both species, and can thus be used to guide conservation management. In this study, we investigate the phylogeographic structure of the Bechstein’s bat, Myotis bechsteinii, and its ectoparasitic bat fly, Basilia nana, at 12 sites across their entire distribution. For both species, a mitochondrial sequence fragment (ND1 and COI respectively) and nuclear microsatellite genotypes (14 and 10 loci respectively) were generated and used to compare the phylogeography of host and parasite. Our findings confirm the presence of three distinct genetic subpopulations of the Bechstein’s bat in (1) Europe, (2) the Caucasus and (3) Iran, which remain isolated from one another. The genetic distinctiveness of host populations in the Caucasus region and Iran emphasize that these populations must be managed as distinct evolutionarily significant units. This phylogeographical pattern is however not reflected in its parasite, B. nana, which shows evidence for more recent dispersal between host subpopulations. The discordant genetic pattern between host and parasite suggest that despite the long-term genetic isolation of the different host subpopulations, long-range dispersal of the parasite has occurred more recently, either as the result of secondary contact in the primary host or via secondary host species. This indicates that a novel pathogenic threat to one host subpopulation may be able to disperse, and thus have important consequences for all subpopulations.


Myotis bechsteinii Basilia nana Nycteribiidae Co-phylogeography Parasite biogeography 



This project was funded by a grant from the Volkswagen Foundation (Az 84959). We thank Ina Römer for her assistance in the lab. We are indebted to the following people for providing samples: Petr Benda, Andrej Conti, Christian Dietz, Peter Estok, Tamas Görföl, Lena Grosche, Frauke Meier, Markus Melber, Collin Morris, Maria Napal, Beytullah Özkan, Serbüllent Pakzus, Boyan Petrov, Sébastien Puechmaille.

Compliance with ethical standards

Sampling of Bechstein’s bats was carried out under license from the responsible nature conservancy departments.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10592_2017_1024_MOESM1_ESM.docx (149 kb)
Supplementary material 1 (DOCX 147 KB)


  1. Arbogast BS, Kenagy GJ (2001) Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr 28:819–825CrossRefGoogle Scholar
  2. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227–227CrossRefPubMedGoogle Scholar
  3. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bruyndonckx N, Biollaz F, Dubey S, Goudet J, Christe P (2010) Mites as biological tags of their hosts. Mol Ecol 19:2770–2778CrossRefPubMedGoogle Scholar
  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  6. Criscione CD (2008) Parasite co-structure: broad and local scale approaches. Parasite 15:439–443CrossRefPubMedGoogle Scholar
  7. Criscione CD, Blouin MS (2007) Parasite phylogeographical congruence with salmon host evolutionarily significant units: implications for salmon conservation. Mol Ecol 16:993–1005CrossRefPubMedGoogle Scholar
  8. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  9. Dekeukeleire D, Janssen R, Haarsma A-J, Bosch T, van Schaik J (2016) Swarming behaviour, catchment area and seasonal movement patterns of the Bechstein’s bats: implications for conservation. Acta Chiropterologica 18:349–358CrossRefGoogle Scholar
  10. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214CrossRefPubMedGoogle Scholar
  11. Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  13. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  14. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  15. Furmankiewicz J, Altringham J (2007) Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites. Conserv Genet 8:913–923CrossRefGoogle Scholar
  16. Galbreath KE, Hoberg EP (2012) Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas. Proc R Soc B 279:371–378CrossRefPubMedGoogle Scholar
  17. Galimberti A, Spada M, Russo D, Mucedda M, Agnelli P, Crottini A, Ferri E, Martinoli A, Casiraghi M (2012) Integrated operational taxonomic units (IOTUs) in echolocating bats: a bridge between molecular and traditional taxonomy. PLoS One, 7:e40122CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gómez-Díaz E, González-Solís J, Peinado MA, Page RDM (2007) Lack of host-dependent genetic structure in ectoparasites of Calonectris shearwaters. Mol Ecol 16:5204–5215CrossRefPubMedGoogle Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  20. Hafner MS, Demastes JW, Spradling TA, Reed DL (2003) Cophylogeny between pocket gophers and chewing lice. In:Page RDM (ed) Tangled trees: phylogeny, cospeciation, and coevolution. University of Chicago Press, Chicago, pp 195–220Google Scholar
  21. Hedrick PW (2005) A standardized genetic differentiation measure. Evol Int J org Evol 59:1633–1638CrossRefGoogle Scholar
  22. Hutson AM, Aulagnier S, Spitzenberger F (2008) Myotis nattereri. The IUCN Red List of Threatened Species 2008; e.T14135A4405996Google Scholar
  23. Jost L (2008) Gst and its relatives do not measure differentiation. Mol Ecol 17:4015–4026CrossRefPubMedGoogle Scholar
  24. Juste J, Ibáñez C, Muñoz J, Trujillo D, Benda P, Karataş A, Ruedi M (2004) Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands. Mol Phylogenet Evol 31:1114–1126CrossRefPubMedGoogle Scholar
  25. Kerth G, Morf L (2004) Behavioral and genetic data suggest that Bechstein’s bat predominately mate outside the breeding habitat. Ethology 110:987–999CrossRefGoogle Scholar
  26. Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein’s bat (Myotis bechsteinii). Mol Ecol 14:3943–3950CrossRefPubMedGoogle Scholar
  27. Kerth G, van Schaik J (2012) Causes and consequences of living in closed societies: lessons from a long-term socio-genetic study on Bechstein’s bats. Mol Ecol 21:633–646CrossRefPubMedGoogle Scholar
  28. Kerth G, Mayer F, Petit E (2002) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein’s bat (Myotis bechsteinii). Mol Ecol 11:1491–1498CrossRefPubMedGoogle Scholar
  29. Kerth G, Kiefer A, Trappmann C, Weishaar M (2003) High gene diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein’s bat. Conserv Genet 4:491–499CrossRefGoogle Scholar
  30. Kerth G, Petrov B, Conti A, Anastasov D, Weishaar M, Gazaryan S, Jaquiery J, Konig B, Perrin N, Bruyndonckx N (2008) Communally breeding Bechstein’s bats have a stable social system that is independent from the postglacial history and location of the populations. Mol Ecol 17:2368–2381CrossRefPubMedGoogle Scholar
  31. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634CrossRefPubMedGoogle Scholar
  32. Levin II, Parker PG (2013) Comparative host-parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds. Parasitology 140:1061–1069CrossRefPubMedGoogle Scholar
  33. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  34. Nabholz B, Glemin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130CrossRefPubMedGoogle Scholar
  35. Nagy ZT, Sonet G, Mortelmans J, Vandewynkel C, Grootaert P (2013) Using DNA barcodes for assessing diversity in the family Hybotidae (Diptera, Empidoidea). ZooKeys 365:263–278Google Scholar
  36. Nieberding CM, Morand S (2007) Comparative phylogeography: the use of parasites for insights into host history. In:Krasnov BR, Morand S, Poulin R (eds) Micromammals and macroparasites: from evolutionary ecology to management. Springer, Tokyo, 277–293Google Scholar
  37. Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology? Trends Ecol Evol 22:156–165CrossRefPubMedGoogle Scholar
  38. Nieberding C, Morand S, Libois R, Michaux JR (2004) A parasite reveals cryptic phylogeographic history of its host. Proc R Soc Lond B 271:2559–2568CrossRefGoogle Scholar
  39. Nieberding CM, Durette-Desset MC, Vanderpoorten A, Casanova JC, Ribas A, Deffontaine V, Feliu C, Morand S, Libois R, Michaux JR (2008) Geography and host biogeography matter for understanding the phylogeography of a parasite. Mol Phylogenet Evol 47:538–554CrossRefPubMedGoogle Scholar
  40. O’Donnell CF, Richter S, Dool S, Monks JM, Kerth G (2016) Genetic diversity is maintained in the endangered New Zealand long-tailed bat (Chalinolobus tuberculatus) despite a closed social structure and regular population crashes. Conserv Genet 17:91–102CrossRefGoogle Scholar
  41. Paunovíc M (2016) Myotis bechsteinii. The IUCN Red List of Threatened Species 2016; e.T14123A22053752Google Scholar
  42. Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc R Soc Lond B 266:1717–1722CrossRefGoogle Scholar
  43. Petit E, Excoffier L, Mayer F (1999) No evidence of bottleneck in the postglacial recolonization of Europe by the noctule bat (Nyctalus noctula). Evolution 53:1247–1258PubMedGoogle Scholar
  44. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  45. Puechmaille SJ, Allegrini B, Boston ESM, Dubourg-Savage M-J, Evin A, Knochel A, Le Bris Y, Lecoq V, Lemaire M, Rist D, Teeling EC (2012) Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex. Mamm Biol 77:224–228CrossRefGoogle Scholar
  46. Rambaut A, Suchard M, Xie W, Drummond A (2014) Tracer v1.6. Institute of Evolutionary Biology, University of Edinburgh, EdinburghGoogle Scholar
  47. Reckardt K, Kerth G (2006) The reproductive success of the parasitic bat fly Basilia nana (Diptera : Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein’s bat (Myotis bechsteinii). Parasitol Res 98:237–243CrossRefPubMedGoogle Scholar
  48. Rivers NM, Butlin RK, Altringham JD (2005) Genetic population structure of Natterer’s bats explained by mating at swarming sites and philopatry. Mol Ecol 14:4299–4312CrossRefPubMedGoogle Scholar
  49. Rousset F (2008) GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  50. Ruedi M, Mayer F (2001) Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Mol Phylogenet Evol 21:436–448CrossRefPubMedGoogle Scholar
  51. Ruedi M, Stadelmann B, Gager Y, Douzery EJ, Francis CM, Lin LK, Guillen-Servent A, Cibois A (2013) Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Mol Phylogenet Evol 69:437–449CrossRefPubMedGoogle Scholar
  52. Stadelmann B, Lin LK, Kunz TH, Ruedi M (2007) Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Mol Phylogenet Evol 43:32–48CrossRefPubMedGoogle Scholar
  53. Szentivanyi T, Estok P, Földvári M (2016) Checklist of host associations of European bat flies (Diptera: Nycteribiidae, Streblidae). Zootaxa 4205:101–126CrossRefGoogle Scholar
  54. Theodor O (1967) An Illustrated Catalogue of the Rothschild Collection of Nycteribiidae (Diptera) in the British Museum (Natural History). Publication 655. London: Trustees of the British Museum (Natural History), 8, 5Google Scholar
  55. Toon A, Hughes JM (2008) Are lice good proxies for host history? A comparative analysis of the Australian magpie, Gymnorhina tibicen, and two species of feather louse. Heredity 101:127–135CrossRefPubMedGoogle Scholar
  56. Topál G (1983) New and rare fossil mouse-eared bats from the Middle Pliocene of Hungary (Mammalia, Chiroptera). Fragmenta Mineralogica et Palaeontologica 11:43–54Google Scholar
  57. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  58. van Schaik J, Dekeukeleire D, Kerth G (2015a) Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species. Mol Ecol 24:2324–2335CrossRefPubMedGoogle Scholar
  59. van Schaik J, Janssen R, Bosch T, Haarsma A-J, Dekker JJA, Kranstauber B (2015b) Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites. PLoS ONE 10:e0130850CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wang J (2017) The computer program structure for assigning individuals to populations: easy to use but easier to misuse. Mol Ecol Resour 17:981–990Google Scholar
  61. Whiteman NK, Kimball RT, Parker PG (2007) Co-phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Mol Ecol 16:4759–4773CrossRefPubMedGoogle Scholar
  62. Wilke T, Schultheiß R, Albrecht C (2009) As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. Am Malacol Bull 27:25–45CrossRefGoogle Scholar
  63. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedPubMedCentralGoogle Scholar
  64. Witsenburg F, Clement L, Lopez-Baucells A, Palmeirim J, Pavlinic I, Scaravelli D, Sevcik M, Dutoit L, Salamin N, Goudet J, Christe P (2015) How a haemosporidian parasite of bats gets around: the genetic structure of a parasite, vector and host compared. Mol Ecol 24:926–940CrossRefPubMedGoogle Scholar
  65. Yavruyan E, Rakhmatulina I, Bukhnikashvili A, Kandaurov A, Natradze I, Gazaryan S (2008) Bats conservation action plan for the Caucasus. Publishing House Universal, TbilisiGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Zoological Institute & MuseumGreifswald UniversityGreifswaldGermany
  2. 2.Department of Behavioural Ecology and Evolutionary GeneticsMax Planck Institute for OrnithologySeewiesenGermany
  3. 3.Department of Biology, Terrestrial Ecology UnitGhent UniversityGhentBelgium
  4. 4.UNEP/EUROBATSBonnGermany
  5. 5.Institute of ZoologyIlia State UniversityTbilisiGeorgia

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