Mammalian Biology

, Volume 92, Issue 1, pp 78–85 | Cite as

Genetic diversity distribution among seasonal colonies of a nectar-feeding bat (Leptonycteris yerbabuenae) in the Baja California Peninsula

  • Maria Clara ArteagaEmail author
  • Rodrigo A. Medellín
  • Patricia Astrid Luna-Ortíz
  • Paul A. HeadyIII
  • Winifred F. Frick
Original investigation


Gene flow and historical demography influence the level and distribution of population genetic variation. The nectar-feeding bat Leptonycteris yerbabuenae is a colonial and migratory species in tropical and subtropical regions of North America. We examined the distribution of genetic diversity among colonies of this species and assess whether a population in Baja California Peninsula shows signature of historical demographic change. We expected low genetic differentiation, because individuals are highly mobile and share mating sites. We also predicted a demographic signature consistent with past climatic fluctuations. During the spring maternity season, we sampled 120 individuals of six colonies along a 450 km transect in the Baja California Peninsula, Mexico. Individuals were genotyped with eight nuclear microsatellite loci and 1739 bp of two mitochondrial markers. We record weak but significant levels of nuclear structure and no mitochondrial differentiation among these colonies suggesting a high level of gene flow mediated by females. Genetic diversity estimation per colony and in the region was moderate, and consistent with previous studies. The mitochondrial data indicate that the population in the Baja California Peninsula experienced a demographic expansion during or after the late Pleistocene, probably related to the expansion of food resources. This is the first detailed genetic population study of L. yerbabuenae on the spatially disjunct part of its geographical range and it is the first record of a demographic expansion in a migratory nectar-feeding bat species from North America. Our results contribute to understanding the past demography and the natural history of this species in the Baja California Peninsula.


Cytochrome b ND1 region Genetic differentiation Historical demography Microsatellites 


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  1. Arita, H., 1991. Spatial segregation in long-nosed bats, Leptonycteris nivalis and Leptonycteris curasoae, in Mexico. J. Mammal. 72, 706–714.CrossRefGoogle Scholar
  2. Baerwald, E.F., Patterson, W.P., Barclay, R.M.R., 2014. Origins and migratory patterns of bats killed by wind turbines in southern Alberta: evidence from stable isotopes. Ecosphere 5, 1–17.CrossRefGoogle Scholar
  3. Baker, R.J., Cockrum, E.L., 1966. Geographic and ecological range of the long-nosed bats, Leptonycteris. J. Mammal. 47, 329–331.CrossRefGoogle Scholar
  4. Bilgin, R., Karataş, A., Çoraman, E., Morales, J.C., 2008a. The mitochondrial and nuclear genetic structure of Myotis capaccinii (Chiroptera: Vespertilionidae) in the Eurasian transition, and its taxonomic implications. Zool. Scr. 37, 253–262.CrossRefGoogle Scholar
  5. Bilgin, R., Karataş, A., Çoraman, E., Disotell, T., Morales, J.C., 2008b. Regionally and climatically restricted patterns of distribution of genetic diversity in a migratory bat species, Miniopterus schreibersii (Chiroptera: Vespertilionidae). BMC Evol. Biol. 8, 209.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Birky, C.W., Maruyama, T., Fuerst, P., 1983. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513–527.PubMedPubMedCentralGoogle Scholar
  7. Bryja, J., Kaňuch, P., Fornsková, A., Bartonička, T., Řehák, Z., 2009. Low population genetic structuring of two cryptic bat species suggests their migratory behaviour in continental Europe. Biol. J. Linn. Soc. 96, 103–114.CrossRefGoogle Scholar
  8. Burns, L.E., Frasier, T.R., Broders, H.G., 2014. Genetic connectivity among swarming sites in the wide ranging and recently declining little brown bat (Myotis lucifugus). Ecol. Evol. 4, 4130–4149.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Castella, V., Ruedi, M., Excoffier, L., Ibáñez, C., 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ceballos, G., Fleming, T.H., Chavez, C., Nassar, J., 1997. Population dynamics of Leptonycteris curasoae (Chiroptera: Phyllostomidae) in Jalisco, Mexico. J. Mammal. 78, 1220–1230.CrossRefGoogle Scholar
  11. Chesser, R.K., Baker, R.J., 1996. Effective sizes and dynamics of uniparentally and biparentally inherited genes. Genetics 144, 1225–1235.PubMedPubMedCentralGoogle Scholar
  12. Clark-Tapia, R., Molina-Freaner, F., 2003. The genetic structure of a columnar cactus with a disjunct distribution: Stenocereus gummosus in the Sonoran desert. Heredity 90, 443–450.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cockrum, E., 1991. Seasonal distribution of northwestern populations ofthe long-nosed bats, Leptonycteris sanborni family Phyllostomidae. An. Inst. Biol. Ser. Zool. 62, 181–202.Google Scholar
  14. Cole, F.R., Wilson, D.E., 2006. Leptonycteris yerbabuenae. Mamm. Species 797, 1–7.CrossRefGoogle Scholar
  15. Datzmann, T., von Helversen, O., Mayer, F., 2010. Evolution of Nectarivory in Phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evol. Biol. 10, 165.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dixon, M.D., 2011. Population genetic structure and natal philopatry in the widespread North American bat Myotis lucifugus. J. Mammal. 92, 1343–1351.CrossRefGoogle Scholar
  17. Dolby, G.A., Bennett, S.E., Lira-Noriega, A., Wilder, B.T., Munguía-Vega, A., 2015. Assessing the geological and climatic forcing of biodiversity and evolution surrounding the Gulf of California. J. Southwest 57, 391–455.CrossRefGoogle Scholar
  18. Evanno, G., Regnault, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14, 2611–2620.CrossRefGoogle Scholar
  19. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinf. 1, 47–50.CrossRefGoogle Scholar
  20. Fleming, T.H., Eby, P., 2003. Ecology of bat migration. In: Kunz, T.H., Fenton, M.B. (Eds.), Bat Ecology. The University of Chicago Press, Chicago, Illinois, pp. 156–208.Google Scholar
  21. Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.PubMedPubMedCentralGoogle Scholar
  22. Goudet, J., Available from URL: 2001. FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices Ver. 2.9.3. Scholar
  23. Grismer, L.L., 2000. Evolutionary biogeography on Mexico’s Baja California Peninsula: a synthesis of molecules and historical geology. Proc. Natl. Acad. Sci. U. S.A. 7, 14017–14018.CrossRefGoogle Scholar
  24. Gutiérrez-Flores, C., 2015. Filogeografía y estructuragenética poblacional del cardón Pachycereus pringlei en el Noroeste de México. In: Thesis. CIBNOR, México.Google Scholar
  25. Hedrick, P.W., 2005. Genetics of Populations, third ed. Jones and Bartlett Publishers, Sudbury, Massachusetts.Google Scholar
  26. Hewitt, G.M., 2004a. Genetic consequences of climatic oscillations in the quaternary. Philos. Trans. R. Soc. Lond. B359, 183–195.CrossRefGoogle Scholar
  27. Hewitt, G.M., 2004b. The structure of biodiversity-insights from molecular phylogeography. Front. Zool. 1,4.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Horner, M.A., Fleming, T.H., Sahley, C.T., 1998. Foraging behaviour and energetics of a nectar-feeding bat Leptonycteris curasoae (Chiroptera: Phyllostomidae). J. Zool. 244, 575–586.CrossRefGoogle Scholar
  29. Johnson, J.A., Toepfer, J.E., Dunn, P.O., 2003. Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens. Mol. Ecol. 12, 3335–3347.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Librado, P., Rozas,J., 2009. DnaSP ver. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle Scholar
  31. Lozano-Garza, O.A., 2013. Análisis de la estructura genética poblacional de la pitaya agria (Stenocereus gummosus) en el Desierto Sonorense. In: Thesis. CIBNOR, México.Google Scholar
  32. McCracken, G.F., McCracken, M.K., Vawter, A.T., 1994. Genetic structure in migratory populations of the bat Tadarida brasiliensis mexicana. J. Mammal. 75, 500–514.CrossRefGoogle Scholar
  33. Mayer, F., von Helversen, O., 2001. Cryptic diversity in European bats. Philos. Trans. R. Soc. Lond. B 268, 1825–1832.Google Scholar
  34. Medellín, R.A., Wiederholt, R., López-Hoffman, L., 2017. Conservation relevance of bat caves for biodiversity and ecosystem services. Biol. Conserv. 211, 45–50.CrossRefGoogle Scholar
  35. Medellín, R.A., 2016a. Leptonycteris yerbabuenae. In: The IUCN Red List of Threatened Species 2016: e.T136659A21988965.,, Downloaded on 05 May 2017.Google Scholar
  36. Medellín, R.A., 2016b. Leptonycteris nivalis. In: The IUCN Red List of Threatened Species 2016: e.T11697A22126172.,, Downloaded on 05 May 2017.Google Scholar
  37. Medellín, R.A., Arita, H., Sánchez, O., 2008. Identificación de los murciélagos de México, Clave de Campo. Instituto de Ecología, UNAM, México D.F.Google Scholar
  38. Morales-Garza, M., Arizmendi, M., Campos, J., Martínez-Garcia, M.Google Scholar
  39. Valiente-Banuet, A., 2007. Evidences on the migratory movements of the nectar-feeding bat Leptonycteris curasoae in Mexico using random amplified polymorphic DNA (RAPD). J. Arid Environ. 68, 248–259.CrossRefGoogle Scholar
  40. Moussy, C., Hosken, D.J., Mathews, F., Smith, G.C., Aegerter, J.N., Bearhop, S., 2013. Migration and dispersal patterns of bats and their influence on genetic structure. Mammal. Rev. 43, 183–195.CrossRefGoogle Scholar
  41. Navascués, M., Vaxevanidou, Z., González-Martínez, S.C., Climent, J., Gil, L., Emerson, B.C., 2006. Chloroplast microsatellites reveal colonization and metapopulation dynamics in the Canary Island pine. Mol. Ecol. 15, 2691–2698.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Peakall, R., Smouse, P.E., 2006. GenALEx 6: genetic analysis in excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.CrossRefGoogle Scholar
  43. Petit, E., Excoffier, L., Mayer, F., 1999. No evidence of bottleneck inthe postglacial recolonization of Europe by the noctule bat (Nyctalus noctula). Evolution, 1247–1258.Google Scholar
  44. 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, 1717–1722.CrossRefGoogle Scholar
  45. Piertney, S.B., MacColl, A.D.C., Bacon, P.J., Racey, P.A., Lambin, X., Dallas, J.F., 2000. Matrilineal genetic structure and femalemediated gene flow in red grouse (Lagopus lagopus scoticus): an analysis using mitochondrial DNA. Evolution 54, 279–289.PubMedPubMedCentralGoogle Scholar
  46. Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  48. Pylant, C.L., Nelson, D.M., Fitzpatrick, M.C., Gates, J.E., Keller, S.R., 2016. Geographic origins and population genetics of bats killed at wind-energy facilities. Ecol. Appl. 26, 1381–1395.CrossRefPubMedPubMedCentralGoogle Scholar
  49. R Core Team, 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  50. Ramirez, Judith, 2011. Population genetic structure of the lesser long-nosed bat (Leptonycteris yerbabuenae) in Arizona and Mexico. Thesis. University of Arizona, Arizona.Google Scholar
  51. Ramirez, J., Munguia-Vega, A., Culver, M., 2011. Isolation of microsatellite loci from the lesser long-nosed bat (Leptonycteris yerbabuenae). Conserv. Genet. Resour. 3, 327–329.CrossRefGoogle Scholar
  52. Ramos-Pereira, M.J., Salgueiro, P., Rodrigues, L., Coelho, M.M., Palmeirim, J.M., 2009. Population structure of a cave-dwelling bat, Miniopterus schreibersii: does it reflect history and social organization? Heredity 100, 533–544.CrossRefGoogle Scholar
  53. Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2) population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.CrossRefGoogle Scholar
  54. Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rogers, A.R., Harpending, H., 1992. Population growth makes waves inthe distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552–569.PubMedPubMedCentralGoogle Scholar
  56. Rogers, A.R., 1995. Genetic evidence fora Pleistocene population explosion. Evolution 49, 608–615.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ruedi, M., Mayer, F., 2001. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Mol. Phylogenet. Evol. 21, 436–448.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Ruedi, M., Castella, V., 2003. Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: a mitochondrial and nuclear survey. Mol. Ecol. 12, 1527–1540.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Russell, A., Turmelle, A., Brown, V., McCracken, G., 2005. Extremely variable di-and tetranucleotide microsatellite loci in Brazilian free-tailed bats (Tadarida brasiliensis). Mol. Ecol. Notes 5, 669–671.CrossRefGoogle Scholar
  60. Salgueiro, P., Ruedi, M., Coelho, M.M., Palmeirim, J.M., 2007. Genetic divergence and phylogeography in the genus Nyctalus (Mammalia, Chiroptera): implications for population history of the insular bat Nyctalus azoreum. Genetica 130, 169–181.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Scheinvar, E., Gámez, N., Castellanos-Morales, G., Aguirre-Planter, E., Eguiarte, L.E., 2017. Neogene and Pleistocene history of Agave lechuguilla in the Chihuahuan desert. J. Biogeogr. 44, 322–334.CrossRefGoogle Scholar
  62. Sikes, R.S., Gannon, W.L., 2011. The animal care and use Committee of the American Society Mammalogists. Guidelines of the American Society of Mammologists fortheuse ofwild animals in research. J. Mammal. 92, 235–253.CrossRefGoogle Scholar
  63. Simmons, N.B., 2005. Chiroptera. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference., third edition. Johns Hopkins University Press, Baltimore, Maryland, pp. 312–529.Google Scholar
  64. Steppan, S.J., Akhverdyan, M.R., Lyapunova, E.A., Fraser, D.G., Vorontsov, N.N., Hoffmann, R.S., Braun, M.J., 1999. Molecular phylogeny of the marmots (Rodentia: Sciuridae): tests of evolutionary and biogeographic hypotheses. Syst. Biol. 48, 715–734.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Stoner, K., Salazar, K.O., Fernández, R.R., Quesada, M., 2003. Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodivers. Conserv. 12, 357–373.CrossRefGoogle Scholar
  66. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Valiente-Banuet, A., Arizmendi, M., Rojas-Martínez, A., Domínguez-Canseco, L., 1996. Ecological relationships between columnar cacti and nectar-feeding bats in Mexico. J. Trop. Ecol. 12, 103–119.CrossRefGoogle Scholar
  68. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.CrossRefGoogle Scholar
  69. Voigt, C.C., Lindecke, O., Schönborn, S., Kramer-Schadt, S., Lehmann, D., 2016. Habitat use of migratory bats killed during autumn at wind turbines. Ecol. Appl. 26, 771–783.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Weyeneth, N., Goodman, S.M., Ruedi, M., 2011. Do diversification models of Madagascar’s biota explain the population structure of the endemic bat Myotis goudoti (Chiroptera: Vespertilionidae)? J. Biogeogr. 38, 44–54.CrossRefGoogle Scholar
  71. Wilkinson, G., Fleming, T., 1996. Migration and evolution of lesser long-nosed bats Leptonycteris curasoae, inferred from mitochondrial DNA. Mol. Ecol. 5, 329–339.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2018

Authors and Affiliations

  • Maria Clara Arteaga
    • 1
    Email author
  • Rodrigo A. Medellín
    • 2
  • Patricia Astrid Luna-Ortíz
    • 1
  • Paul A. HeadyIII
    • 3
  • Winifred F. Frick
    • 4
    • 5
  1. 1.Departamento de Biología de la ConservaciónCentro de Investigación Científica y de Educación Superior de Ensenada (CICESE)EnsenadaMéxico
  2. 2.Departamento de Ecología de la Biodiversidad, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMéxico Distrito FederalMéxico
  3. 3.Bat Conservation Research and ServicesAptosUSA
  4. 4.Ecology and Evolutionary BiologyUniversity of CaliforniaSanta CruzUSA
  5. 5.Bat Conservation InternationalAustinUSA

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