Skip to main content

Advertisement

Log in

Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Plecotus auritus, a small, gleaning bat species, lives in small, isolated summer colonies in which both males and females show a high degree of natal philopatry. Despite this, colonies have high gene diversities and low inbreeding coefficients. It has been suggested that inbreeding is avoided because mating occurs during autumnal and spring swarming at hibernation sites. We tested this hypothesis by comparing microsatellite profiles, based on eight loci, of bats from six summer colonies and two swarming sites they were known to visit from radiotelemetry studies. We found high gene diversities (Hs = 0.77) at both swarming sites and summer colonies which were not statistically different. There was no detectable isolation by distance and FST was low (0.001). Together, these results suggest high gene flow between sites. Despite this, there was small but significant genetic differentiation amongst summer colonies and between summer colonies and the primary swarming site. We suggest that swarming is important for gene flow and for maintaining genetic diversity in this highly philopatric species and discuss possible reasons for the genetic differentiation observed. The identification and protection of swarming sites should be a major conservation priority for this and other temperate bat species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Bauerová Z, Zima J (1988) Seasonal changes in visits to a cave by bats. Fol. Zool 37:97–111

    Google Scholar 

  • Burland TM, Barratt EM, Racey PA (1998) Isolation and characterization of microsatellite loci in the brown long-eared bat, Plecotus auritus, and cross-species amplification in the family Vespertilionidae. Mol Ecol 7:136–138

    CAS  Google Scholar 

  • Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc R Soc London Ser B 266:975–980

    Article  Google Scholar 

  • Burland TM, Worthington Wilmer J (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409

    Article  PubMed  CAS  Google Scholar 

  • Castella V, Ruedi M (2000) Characterization of highly variable microsatellite loci in the bat Myotis myotis (Chiroptera: Vespertilionidae). Mol. Ecol 9:1000–1002

    Article  PubMed  CAS  Google Scholar 

  • Castella VM, Ruedi L, Excoffier C, Ibanez R, Arlettaz R, Hausser J (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Mol Ecol 9:1761–1772

    Article  PubMed  CAS  Google Scholar 

  • Davis WH, Hitchcock HB (1965) Biology and migration of the bat Myotis lucifugus in New England. J Mammal 46:296–313

    Article  Google Scholar 

  • Entwistle AC, Racey PA, Speakman JR (1996) Habitat exploitation by a gleaning bat, Plecotus auritus. Phil Trans R Soc London B 351:921–931

    Article  Google Scholar 

  • Entwistle AC, Racey PA, Speakman JR (2000) Social and population structure of a gleaning bat, Plecotus auritus. J Zool 252:11–17

    Article  Google Scholar 

  • Fenton MB (1969) Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Can J Zool 47:597–602

    Google Scholar 

  • Fuhrmann M Seitz A (1992) Nocturnal activity of the brown long-eared bat (Plecotus auritus L., 1758): data from radiotracking in the Lenneberg forest near Mainz (Germany). In: Priede IG, Swift SM (eds), Wildlife Telemetry. Remote monitoring and tracking of animals Ellis Horwood, Chichester, pp 538–548

    Google Scholar 

  • Furmankiewicz J (2002) Mating behaviour of the brown long-eared bat Plecotus auritus. Bat Res News 43:84–85

    Google Scholar 

  • Furmankiewicz J (2004) Mating behaviour of brown long-eared bat Plecotus auritus (Linnaeus, 1758). PhD thesis, University of Wroclaw, Poland. [in Polish]

  • Furmankiewicz J (2005) Social calls and vocal activity of the brown long-eared bat Plecotus auritus in SW Poland. Le Rhinolophe 17:101–120

    Google Scholar 

  • Furmankiewicz J, Górniak J (2002) Seasonal changes in number and diversity of bat species (Chiroptera) in the Stolec mine (SW Poland). Przyr Sud Zach, Supplement 2:49–70

    Google Scholar 

  • Gaisler J, Hanák V, Hanzal V, Jarský V (2003) Výsledky kroužkování netopýrů v České republice a na Slovensku, 1948–2000. Vespertilio 7:3–61

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html

  • Hall JS, Brenner FJ (1965) A behaviour of bats, not related to roosting, in the use of caves in summer. Am Zool 5:225

    Google Scholar 

  • Hall JS, Brenner FJ (1968) Summer netting of bats at a cave in Pensylvania. J Mammal 49(4):779–781

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population level. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Horáček I (1975) Notes on the ecology of bats of the genus Plecotus Geoffroy, 1818 (Mammalia: Chiroptera). Vest Cs Spol Zool 3:195–210

    Google Scholar 

  • Horáček I, Zima J (1978) Net-revealed cave visitation and cave-dwelling in European bats. Folia Zool 27:135–148

    Google Scholar 

  • Humphrey SR, Cope JB (1976) Population ecology of the Little Brown Bat Myotis lucifugus, in Indiana and North-central Kentucky. Special Publication of the American Society of Mammalogists, Oklahoma

    Google Scholar 

  • Kerth G, Mayer F, König B (2000) Mitochondrial DNA (mtDNA) reveals that female Bechstein’s bats live in close societies. Mol Ecol 9:793–800

    Article  PubMed  CAS  Google Scholar 

  • Kerth G, Mayer F, Petit E (2002a) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein’s bat (Myotis bechsteinii). Mol Ecol 11:1491–1498

    Article  CAS  Google Scholar 

  • 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). Behav Ecol Sociobiol 52:203–210

    Article  Google Scholar 

  • Kerth G, Kiefer A, Trappmann C, Weishaar M (2003) High gene diversity at swarming sites suggests hot spots for gene flow in the endangered Bechstein’s bat. Cons Genet 4:491–499

    Article  CAS  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17(4):183–189

    Article  Google Scholar 

  • Lowe A, Harris S, Ashton P (2004) Ecological genetics: design, analysis, and application. Blackwell Publishing, Oxford

    Google Scholar 

  • Masing M (1989) Bat research and bat protection in Estonia. In: Hanak V, Horaček I, Gaisler J (eds.), European bat research 1987, vol 1987. Charles University Press, Praha pp 343–347

    Google Scholar 

  • McCracken G F (1984) Social organization and genetic variation in two species of emballonurid bats. Z Tierpsychol 66:55–69

    Google Scholar 

  • Miller-Butterworth CM, Jacobs DS, Harley EH (2003) Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature 424(6945):187–191

    Article  PubMed  CAS  Google Scholar 

  • Moffat CB (1922) The habits of the long-eared bat. Irish Nat 31:105–111

    Google Scholar 

  • Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Phil Trans R Soc London B 316:335–427

    Article  Google Scholar 

  • Paetkau D, Slades D, Burden M, 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 13:55–56

    Article  PubMed  CAS  Google Scholar 

  • Parsons KN, Jones G (2003) Dispersion and habitat use by Myotis daubentonii and Myotis nattereri during the swarming season: implication for conservation. Anim Conserv 6:283–290

    Article  Google Scholar 

  • Parsons KN, Jones G, Davidson-Watts I, Greenaway F (2003) Swarming of bats at underground sites in Britain – implications for conservation. Biol Conserv 111:63–70

    Article  Google Scholar 

  • Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc Roy Soc London Ser B 266:1717–1722

    Article  CAS  Google Scholar 

  • Petit E, Mayer F (2000) A population genetic analysis of migration: the case of noctule bat (Nyctalus noctula). Mol Ecol 9:683–690

    Article  PubMed  CAS  Google Scholar 

  • Petri B, Pääbo S, von Haeseler A, Tautz D (1997) Paternity assessment and population subdivision in a natural population of the larger mouse-eared bat Myotis myotis. Mol. Ecol 6:235–242

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: A software for genetic assignment and first-generation migrant detection. http://www.montpellier.inra.fr/CBGP/softwares/index.htm. J Hered 95:536–539

  • Pugh M, Altringham JD (2005) The effect of gates on cave entry by swarming bats. Acta Chiropterol 7:293–299

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Nat Acad Sci USA 94:9197–9201

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rivers NM, Butlin RK, Altringham JD (2005) Genetic population structure of Natterer’s bats explained by mating at swarming sites and philopatry. Mol Ecol 14:4299–4312

    Article  PubMed  CAS  Google Scholar 

  • Rivers NM, Butlin RK, Altringham JD (2006) Autumn swarming behaviour of Natterer’s bats in the UK: Population size, catchment area and dispersal. Biol Conserv 27:215–226

    Article  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barratt EM (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proc R Soc London Ser B 268:1055–1061

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Senior P, Butlin RK, Altringham JD (2005) Sex and segregation in temperate bats. Proc R Soc London Ser B 272:2467–2473

    Article  Google Scholar 

  • Stebbings RE (1966) A population structure of bats of the Genus Plecotus. J Zool 150:53–75

    Article  Google Scholar 

  • Stebbings RE (1970) A comparative study of Plecotus auritus and P. austriacus (Chiroptera, Vespertilionidae) inhabiting one roost. Proceedings 2nd international bat research conference. Bijdr Tot Dierk 40:91–94

    Google Scholar 

  • Thomas DW, Fenton MB, Barclay RMR (1979) Social behaviour of the Little Brown Bat, Myotis lucifugus. I. Mating behaviour. Behav Ecol Sociobiol 6:129–136

    Article  Google Scholar 

  • Veith M, Kiefer A, Johannesen J, Seitz A (2004) The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus). Heredity 93:342–349

    Article  PubMed  CAS  Google Scholar 

  • Watt EM, Fenton MB (1995) DNA fingerprinting provides evidence of discriminate suckling and non-random mating in little brown bats Myotis lucifugus. Mol Ecol 4:261–264

    PubMed  CAS  Google Scholar 

  • Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unravelling migratory connectivity. Trends Ecol Evol 17(2):76–83

    Article  Google Scholar 

  • Wilkinson GS, Fleming TH (1996) Migration and evolution of lesser long-nosed bats Leptonycteris curasoae, inferred from mitochondrial DNA. Mol Ecol 5(3):329–339

    Article  PubMed  CAS  Google Scholar 

  • Worthington Wilmer JM, Barrat EM (1996) A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res News 37:1–3

    Google Scholar 

Download references

Acknowledgements

The study was funded by the Institute of Zoology, University of Wrocław, Polish State Committee for Scientific Research and a European Marie Curie Training Fellowship. Molecular analysis was done at the University of Leeds and University of Sheffield (Sheffield Molecular Genetics Facility). Bats were caught and sampled under licences from the Polish Environmental Ministry and the local Nature Council. We thank Andy Krupa and Lisa Pope from the NERC Sheffield Molecular Genetics Facility. Roger Butlin helped with lab work and data analysis and gave invaluable assistance with the manuscript. We also are very grateful to our friends, who helped with field work, especially to Marek Furmankiewicz, Katarzyna Duma and Katarzyna Mielcarek. Thank you to all building owners for access to summer roosts and support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna Furmankiewicz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Furmankiewicz, J., Altringham, J. Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites. Conserv Genet 8, 913–923 (2007). https://doi.org/10.1007/s10592-006-9246-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9246-2

Keywords