Conservation Genetics

, Volume 10, Issue 1, pp 143–159 | Cite as

Intraspecific comparison of population structure, genetic diversity, and dispersal among three subspecies of Townsend’s big-eared bats, Corynorhinus townsendii townsendii, C. t. pallescens, and the endangered C. t. virginianus

  • Antoinette J. Piaggio
  • Kirk W. Navo
  • Craig W. Stihler
Research Article


Townsend’s big-eared bat, Corynorhinus townsendii, is distributed broadly across western North America and in two isolated, endangered populations in central and eastern United States. There are five subspecies of C. townsendii; C. t. pallescens, C. t. australis, C. t. townsendii, C. t. ingens, and C. t. virginianus with varying degrees of concern over the conservation status of each. The aim of this study was to use mitochondrial and microsatellite DNA data to examine genetic diversity, population differentiation, and dispersal of three C. townsendii subspecies. C. t. virginianus is found in isolated populations in the eastern United States and was listed as endangered under the Endangered Species Act in 1979. Concern also exists about declining populations of two western subspecies, C. t. pallescens and C. t. townsendii. Using a comparative approach, estimates of the genetic diversity within populations of the endangered subspecies, C. t. virginianus, were found to be significantly lower than within populations of the two western subspecies. Further, both classes of molecular markers revealed significant differentiation among regional populations of C. t. virginianus with most genetic diversity distributed among populations. Genetic diversity was not significantly different between C. t. townsendii and C. t. pallescens. Some populations of C. t. townsendii are not genetically differentiated from populations of C. t. pallescens in areas of sympatry. For the western subspecies gene flow appears to occur primarily through male dispersal. Finally, geographic regions representing significantly differentiated and genetically unique populations of C. townsendii virginianus are recognized as distinct evolutionary significant units.


Corynorhinus townsendii virginianus Mitochondrial DNA Microsatellite DNA Endangered species Genetic diversity 



Lab work for this research was primarily done at the University of Colorado, Boulder by AJP. We would like to thank the following institutions and individuals for tissue samples: Colección Regional Durango (Vertebrados), CIIDIR Durango, Instituto Politécnico Nacional, Celia López-González; Colorado Division of Wildlife, Bats/Inactive Mines Project, Tom Ingersoll, Carole Wilkey, Lea Bonewell, Nancy Olson, Cyndi Mosch; Kentucky Department of Fish and Wildlife Resources, Traci Wethington; Museum of Southwestern Biology; USGS BRD, Michael Bogan, Ernie Valdez; US Fish and Wildlife Service, Robert Currie and Heather Bell; West Virginia Division of Natural Resources; Josh Johnson; Rick Reynolds; Rafael Avila-Flores. We also thank David Armstrong, Robert Guralnick, Susan Perkins, and Kate Huyvaert for their review and comments. This study was partially supported by the Colorado Division of Wildlife, the American Museum of Natural History Theodore Roosevelt Memorial Grant, the American Society of Mammalogists Committee on Grants-in-Aid, the University of Colorado Museum William Henry Burt Grant, the University of Colorado Department of Ecology and Evolutionary Biology, and a Colorado Chapter of the Wildlife Society Grant.


  1. Avise JC (1995) Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv Biol 9:686–690CrossRefGoogle Scholar
  2. Bagley FM (1984) A recovery plan for the Ozark big-eared bat and the Virginia big-eared bat. US Fish and Wildlife Service, Twin Cities, MinnesotaGoogle Scholar
  3. Balloux F, Goudet J, Perrin N (1998) Breeding system and genetic variance in the monogamous, semi-social shrew, Crocidura russula. Evolution 52:1230–1235CrossRefGoogle Scholar
  4. Barbour RW, Davis WH (1969) Bats of America. University of Kentucky Press, Lexington, KentuckyGoogle Scholar
  5. Bourgain C, Abney M, Schneider D, Ober C, McPeek MS (2004) Testing for Hardy-Weinberg Equilibrium in samples with related individuals. Genetics 168:2349–2361PubMedCrossRefGoogle Scholar
  6. Bradbury JW (1977) Social organization and communication. In: Wimsatt WA (eds) Biology of Bats, vol 3. Academic Press, New York. pp 1–72Google Scholar
  7. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455PubMedCrossRefGoogle Scholar
  8. Burland TM, Barrrat EM, Racey PA (1998) Isolation and characterization of microsatellite loci in the brown long-eared bat, Plecotus auritus, and cross-species amplification within the family Vespertilionidae. Mol Ecol 7:133–140CrossRefGoogle Scholar
  9. Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in the gleaning bat, Plecotus auritus. Proc R Soc Lond B Biol Sci 266:975–980CrossRefGoogle Scholar
  10. Burland TM, Wilmer JW (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409PubMedCrossRefGoogle Scholar
  11. Clark MK, Lee DS (1987) Big-eared bat, Plecotus townsendii, in western North Carolina. Brimleyana 13:137–140Google Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 3:1183–1192Google Scholar
  14. Entwistle AC, Racey PA, Speakman JR (2000) Social and population structure of a gleaning bat, Plecotus auritus. J Zool (Lond) 252:11–17CrossRefGoogle Scholar
  15. Fellers GM, Pierson ED (2002) Habitat use and foraging behavior of Townsend’s big-eared bat (Corynorhinus townsendii) in coastal California. J Mammal 83:167–177CrossRefGoogle Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  17. Glaubitz JC (2004) CONVERT: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310CrossRefGoogle Scholar
  18. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995). Available from
  19. Greenwood PJ (1980) Mating systems and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  20. Handley CO (1959) A revision of the American bats of the genera Euderma and Plecotus. Proc U S Natl Mus 110:95–246Google Scholar
  21. Hasegawa M, Kishino H, Yano T (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  22. Hoofer SR, van den Bussche RA (2001) Phylogenetic relationships of plecotine bats and allies based on mitochondrial ribosomal sequences. J Mammal 82:131–137CrossRefGoogle Scholar
  23. Humphrey SR, Kunz TH (1976) Ecology of a Pleistocene relict, the western big-eared bat (Plecotus townsendii) in the southern Great Plains. J Mammal 57:470–494CrossRefGoogle Scholar
  24. Jones C, Suttkus RD (1975) Notes on the natural history of Plecotus rafinesquii. Occas Pap Mus Zool LA State Univ 47:1–14Google Scholar
  25. Kerth G, Mayer F, Konig B (2000) Mitochondrial DNA (mtDNA) reveals that female Bechstein’s bats live in closed societies. Mol Ecol 9:793–800PubMedCrossRefGoogle Scholar
  26. Kunz TH, Martin RA (1982) Plecotus townsendii. Mamm Species 175:1–6Google Scholar
  27. Marjoram P, Donnelly P (1994) Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution. Genetics 136:673–683PubMedGoogle Scholar
  28. Mayer F, Schlotterer C, Tautz D (2000) Polymorphic microsatellite loci in vespertilionid bats isolated from the noctule bat Nyctalus noctula. Mol Ecol 9:2208–2212PubMedCrossRefGoogle Scholar
  29. McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, San Diego, California, pp 321–362CrossRefGoogle Scholar
  30. Menzel MA, Menzel JM, Ford WM, Edwards JW, Carter TC, Churchill JB, Kilgo JC (2001) Home range and habitat use of male Rafinesque’s big-eared bats (Corynorhinus rafinesquii). Am Midl Nat 145:402–408CrossRefGoogle Scholar
  31. Miller-Butterworth CM, Jacobs DS, Harley EH (2003) Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature 424:187–191PubMedCrossRefGoogle Scholar
  32. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  33. Mossman CA, Waser PM (1999) Genetic detection of sex-biased dispersal. Mol Ecol 8:1063–1067PubMedCrossRefGoogle Scholar
  34. Navo KW (1993) Update on Colorado’s bats/inactive mines project. Bat Res News 34:69Google Scholar
  35. Navo KW (1994) Guidelines for the survey of caves and abandoned mines for bats in Colorado. Colorado Division of Wildlife, Monte Vista, COGoogle Scholar
  36. Nei M (1987). Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  37. Neubaum MA, Douglas MR, Douglas ME, O’Shea TJ (2007) Molecular ecology of the big brown bat (Eptesicus fuscus): genetic and natural history variation in a hybrid zone. J Mammal 88:1230–1238CrossRefGoogle Scholar
  38. Pearson OP, Koford MR, Pearson AK (1952) Reproduction of the lump-nosed bat (Corynorhinus rafinesquei) in California. J Mammal 33:273–320CrossRefGoogle Scholar
  39. Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc R Soc Lond B Biol Sci 266:1717–1722CrossRefGoogle Scholar
  40. Petit E, Mayer F (2000) A population genetic analysis of migration: the case of the noctule bat (Nyctalus noctula). Mol Ecol 9:683–690PubMedCrossRefGoogle Scholar
  41. Petit E, Balloux F, Goudet J (2001) Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55:635–640PubMedCrossRefGoogle Scholar
  42. 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 6:235–242PubMedCrossRefGoogle Scholar
  43. Piaggio AJ, Perkins SL (2005) Molecular phylogeny of North American long-eared bats (Vespertilionidae: Corynorhinus): inter- and intraspecific relationships inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 37:762–775PubMedCrossRefGoogle Scholar
  44. Pierson ED, Wackenhut MC, Altenbach JS et al (1999) Species conservation assessment and strategy for Townsend’s big-eared bat (Corynorhinus townsendii townsendii and Corynorhinus townsendii pallescens). Idaho Conservation Effort, Idaho Department of Fish and Game, Boise, IDGoogle Scholar
  45. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  46. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  47. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  48. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  49. Sherwin RE, Stricklan D, Rogers DS (2000a) Roosting affinities of Townsend’s big-eared bat (Corynorhinus townsendii) in northern Utah. J Mammal 81:939–947CrossRefGoogle Scholar
  50. Sherwin RE, Gannon WL, Altenbach JS, Stricklan D (2000b) Roost fidelity of Townsend’s big-eared bat in Utah and Nevada. Trans West Sect Wildl Soc 36:15–20Google Scholar
  51. Sherwin RE, Gannon WL, Altenbach JS (2003) Managing complex systems simply: understanding inherent variation in the use of roosts by Townsend’s big-eared bat. Wildl Soc Bull 3:62–72Google Scholar
  52. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  53. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  54. Smith H, Chiszar D, Montanucci R (1997) Subspecies and classification. Herpetol Rev 28:13–16Google Scholar
  55. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  56. Stihler CW, Jones A, Wallace JL (1997) Use of Elkhorn Cave, Grant County, West Virginia, by a bachelor colony of Corynorhinus townsendii virginianus (abstract). Bat Res News 38:130Google Scholar
  57. Storz JF (2000) Variation at tri- and tetranucleotide repeat microsatellite loci in the fruit bat genus Cynopterus (Chiroptera: Pteropodidae). Mol Ecol 9:2199–2201CrossRefGoogle Scholar
  58. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  59. Szewczak JM, Szewczak SM, Morrison ML, Hall LS (1998) Bats of the White and Inyo Mountains of California-Nevada. Great Basin Nat 58:66–75Google Scholar
  60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  61. Tuttle MD (1977) Gating as a means of protecting cave dwelling bats. In: Ailey T, Rhodes D (eds) National Cave Management Symposium Proceedings. Speleobooks, Albuquerque, New Mexico pp 77–82Google Scholar
  62. Tuttle MD, Taylor DAR (1994) Bats and mines. Resource Publication Bat Conser Int 3:1–41Google Scholar
  63. United States Fish and Wildlife Service (1979) Endangered and threatened wildlife and plants; listing of the Virginia and Ozark Big-Eared Bats as endangered species, and critical habitat determination. Fed Regist 44:69206–69208Google Scholar
  64. United States Fish and Wildlife Service (1989) Endangered and Threatened Wildlife and Plants; Animal Candidate Review for Listing as Endangered or Threatened Species. Fed Regist 54:54554–54579Google Scholar
  65. United States Fish and Wildlife Service (1994) Endangered and Threatened Wildlife and Plants; Animal Candidate Review for Listing as Endangered or Threatened Species. Fed Regist 59:58988Google Scholar
  66. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535CrossRefGoogle Scholar
  67. Vonhof MJ, Davis CS, Fenton MB, Strobeck C (2002) Characterization of dinucleotide microsatellite loci in big brown bats (Eptesicus fuscus), and their use in other North American verspertilionid bats. Mol Ecol Notes 2:167–170CrossRefGoogle Scholar
  68. Weber JL, Wong C (1993) Mutation of human short tandem repeats. Hum Mol Genet 2:1123–1128PubMedCrossRefGoogle Scholar
  69. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  70. Western Bat Working Group (1998) The western bat species: regional priority matrix. Western Bat Working Group. Reno, NevadaGoogle Scholar
  71. Weyandt SE, van den Bussche R, Hamilton MJ, Leslie DM (2005) Unraveling the effects of sex and dispersal: conservation genetics of the endangered Ozark big-eared bat (Corynorhinus townsendii ingens). J Mammal 85:140–148Google Scholar
  72. Wilmer JW, Barratt E (1996) A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res News 37:1–4Google Scholar
  73. Wilmer JW, Moritz C, Hall L, Toop J (1994) Extreme population structuring in the threatened ghost bat, Macroderma gigas: evidence from mitochondrial DNA. Proc R Soc Lond B Biol Sci 257:193–198CrossRefGoogle Scholar
  74. Wilmer JW, Hall L, Barratt E, Moritz C (1999) Genetic structure and male-mediated gene flow in the ghost bat (Macroderma gigas). Evolution 53:1582–1591CrossRefGoogle Scholar
  75. Yang Z, Goldman N, Friday A (1994) Comparison of models for nucleotide substitution used in maximum likelihood phylogenetic estimation. Mol Biol Evol 11:316–324PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Antoinette J. Piaggio
    • 1
    • 2
  • Kirk W. Navo
    • 3
  • Craig W. Stihler
    • 4
  1. 1.USDA/APHIS/WS/National Wildlife Research Center, Wildlife Genetics LabFort CollinsUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of Colorado, BoulderBoulderUSA
  3. 3.Colorado Division of WildlifeMonte VistaUSA
  4. 4.West Virginia Division of Natural ResourcesElkinsUSA

Personalised recommendations