Mammalian Biology

, Volume 84, Issue 1, pp 1–11 | Cite as

Spatial distribution of microsatellite and MHC-DRB exon 2 gene variability in the Jamaican fruit bat (Artibeus jamaicensis) in Mexico

  • Melina Del Real-Monroy
  • Jorge OrtegaEmail author
Original Investigation


Genetic diversity is essential to the evolutionary and adaptive potential of a species. Several empirical genetic studies have highlighted the importance of considering both neutral and adaptive genetic variation when characterizing microevolutionary dynamics. Genes at the major histocompatibility complex (MHC) have become excellent models for researching adaptive variation and natural selection, because of the crucial role they play against pathogens. The Jamaican fruit bat, Artibeus jamaicensis, is one of the most common and well-studied Neotropical mammals and is characterized by generalist feeding habits, high dispersal capability, and abundant populations. Fifteen localities ofArtibeus jamaicensis were genetically assessed using ten neutral microsatellites and one expressed MHC class II locus (DRB) in order to detect footprints of balancing selection. Extensive polymorphism was found at both markers. Overall, 161 alleles were identified at DRB exon 2 gene, and 315 at microsatellites. The observed and expected heterozygosity averaged over all localities ( ±SD) was 0.756 ± 0.15 and 0.885 ± 0.11, respectively, with all localities in Hardy-Weinberg equilibrium. Pairwise genetic differentiation estimates were generally significant, but the overall differentiation was lower at DRB gene (Fst = 0.039) than at microsatellites (Fst = 0.154). We detected significant isolation by distance at microsatellite loci, but not at DRB exon 2 gene. STRUCTURE and BAPS analyses detected a population genetic structure made up of five defined clusters. Our results suggest that balancing selection has maintained the allele frequencies of DRB exon 2 gene across the distribution of A. jamaicensis in Mexico.


Adaptive variation Balancing selection Genetic structure Neotropical bat 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aguilar, A., Garza, J.C., 2006. A comparison of variability and population structure for major histocompatibility complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykis Walbaum). Mol. Ecol 15, 923–937.PubMedCrossRefGoogle Scholar
  2. Alcaide, M., Edwards, S.V., Negro, J.J., Serrano, D., Tella, J., 2008. Extensive polymorphism and geographical variation at a positively selected MHC class II Bgene of the lesser kestrel (Falco naumanni). Mol. Ecol 17, 2652–2665.PubMedCrossRefGoogle Scholar
  3. Aljanabi, S., Martinez, I., 1997. Universal and rapid salt extraction of high quality genomic DNA for PCR-based techniques. Nucl. Acid Res 25, 4692–4693.CrossRefGoogle Scholar
  4. Bernatchez, L., Landry, C., 2003. MHC studies in non-model vertebrates: what have we learned about natural selection in 15 years? J. Evol. Biol 16, 363–377.CrossRefGoogle Scholar
  5. Burland, T.M., Barratt, E.M., Beaumont, M.A., Racey, P.A., 1999. Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc. R. Soc 266, 975–980.CrossRefGoogle Scholar
  6. Cammen, K., Hoffman, J.I., Knapp, L.A., Harwood, J., Amos, W., 2011. Geographic variation of the major histocompatibility complex in Eastern Atlantic gray seals (Halichoerus gypus). Mol. Ecol 20, 740–752.PubMedCrossRefGoogle Scholar
  7. Consuegra, S., Eyto, E., McGinnity, P., Stet, R.J.M., Jordan, W.C., 2011. Contrasting responses to selection in class I and class Iia mayor histocompatibility complex-linked marker in salmon. Heredity 107, 143–154.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Corander, J., Marttinen, P., 2006. Bayesian identification of admixture events using multilocus molecular markers. Mol. Ecol 15, 2833–2843.PubMedCrossRefGoogle Scholar
  9. Corander, J., Waldmann, P., Sillanpaa, M.J., 2003. Bayesian analysis of genetic differentiation between populations. Genetics 163, 367–374.PubMedPubMedCentralGoogle Scholar
  10. Coscia, I., Vogiatzi, E., Kotoulas, G., Tsigenopoulos, C.S., Mariani, S., 2012. Exploring neutral and adaptive processes in expanding population of gilthead sea bream, Sparus aurata L., in the North-East Atlantic. Heredity 108, 537–546.PubMedCrossRefGoogle Scholar
  11. Cutrera, A., Lacey, E., 2006. Major histocompatibility complex variation in Talas tuco-tucos: the influence ofdemography on selection. J. Mammal 87, 706–716.CrossRefGoogle Scholar
  12. Davis, J.C., 1986. Statistics and Data Analysis in Geology. John Wiley & Sons.Google Scholar
  13. Del Real-Monroy, M., Martinez-Mendez, N., Ortega, J., 2014. MHC-DRB exon 2 diversity of Jamaican-eating bat (Artibeus jamaicensis) from Mexico. Acta Chiropt 16, 301–314.CrossRefGoogle Scholar
  14. Ekblom, S.A., Seather, P., Jacobsson, P., Fiske, T., Sahlman, M., Grahn, J.A., Kalas, J., Höglund, J., 2007. Spatial pattern of MHC class II variation in thegreat snipe (Galllinago media). Mol. Ecol 16, 1439–1451.PubMedCrossRefGoogle Scholar
  15. Estrada, A., Coates-Estrada, R., 2002. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island of Los Tuxtlas, Mexico. Biol. Conserv 103, 237–245.CrossRefGoogle Scholar
  16. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the numberof clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol 14, 2611–2620.PubMedCrossRefGoogle Scholar
  17. Evans, M., Neff, B., Heath, D., 2010. MHC genetic structure and divergence across population of Chinook salmon (Oncorhynchus tshawytscha). Heredity 104, 449–456.PubMedCrossRefGoogle Scholar
  18. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50.CrossRefGoogle Scholar
  19. Excoffier, L., Hofer, T., Foll, M., 2009. Detecting loci under selection in a hierarchically structured population. Heredity 103, 285–298.PubMedCrossRefGoogle Scholar
  20. Falush, D., Stephens, M., Pritchard, J.K., 2007. Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol. Ecol. Notes 7, 574–578.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Figueroa, F., Gunther, E., Klein, J., 1988. MHC polymorphism pre-dating speciation. Nature 335, 265–267.PubMedCrossRefGoogle Scholar
  22. Goudet, J., 1995. FSTAT (Version 1.2): a computer program to calculate F-Statistics. J. Hered 86, 485–486.CrossRefGoogle Scholar
  23. Guillot, G., Leblois, R., Coulon, A., Frantz, C., 2009. Statistical methods in spatial genetics. Mol. Ecol 18, 4734–4756.PubMedCrossRefGoogle Scholar
  24. Guo, S.W., Thomposon, E.A., 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 4, 361–372.CrossRefGoogle Scholar
  25. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron 4, 9.Google Scholar
  26. Henry, M., Cosson, J.F., Pons, J.M., 2007. Abundance may be a misleading indicator of fragmentation-sensivity: the case of fig-eating bats. Biol. Conserv 139, 462–467.CrossRefGoogle Scholar
  27. Hill, G.E., 1991. Plumage coloration is a sexually selected indicator of male quality. Nature 350, 337–339.CrossRefGoogle Scholar
  28. Hubisz, M.J., Falush, D., Stephens, M., Pritchard, J.K., 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour 9, 1322–1332.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Jumbart, T., Pontier, D., Dufour, A.B., 2009. Genetic markers in the playground of multivariate analysis. Heredity 102, 330–341.CrossRefGoogle Scholar
  30. Landry, C., Bernatchez, L., 2001. Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol. Ecol 10, 2525–2539.CrossRefGoogle Scholar
  31. Lukas, D., Bradley, B.J., Nsubuga, A.M., Doran-Sheehy, D., Robbins, M.M., Vigilant, L., 2004. Major histocompatibility complex and microsatellite variation in two populations of wild gorillas. Mol. Ecol. 13, 3389–3402.CrossRefGoogle Scholar
  32. Manly, B.F.J., 1985. The Statistics of Natural Selection on Animal Populations. Chapman & Hall, London.Google Scholar
  33. Mayer, F., Brunner, A., 2007. Non-neutral evolution of the major histocompatibility complex class II gene DRB1 in the sac-winged bat Saccopteryx bilineata. Heredity 99, 257–264.PubMedCrossRefGoogle Scholar
  34. Maynard-Smith, J., Haigh, J., 1974. The hitchhiking effect of a favourable gene. Genet. Res. Camb 23, 23–35.CrossRefGoogle Scholar
  35. McConnell, T.J., Godwin, U.B., Cuthbertson, B.J., 1998. Expressed major histocompatibility complex class II loci in fishes. Immunol. Rev 166, 294–300.PubMedCrossRefGoogle Scholar
  36. 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
  37. Medellin, R.A., Arita, H., Sánchez, O., 2008. Identificación de los murciélagos de México, Clave de Campo. Instituto de Ecología, UNAM, México, D.F, 79 pp.Google Scholar
  38. Muirhead, C.A., 2001. Consequences of population structure ongenes under balancing selection. Evolution 55, 1532–1541.PubMedCrossRefGoogle Scholar
  39. Muscarella, R.A., Murray, K.L., Ortt, D., Russell, A.L., Fleming, T.H., 2011. Exploring demographic, physical, and historical explanations for the genetic structure of two lineages of Greater Antillean bats. PLoS One 6, e17704.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Nadachowska-Brzyska, K., Zeilinski, P., Radwan, J., Babik, W., 2012. Interspecific hybridization increases MHC class II diversity in two sisterspecies of newts. Mol. Ecol 21, 887–906.CrossRefGoogle Scholar
  41. Nielsen, R., 2001. Statistical test of selective neutrality in the age of genomics. Heredity 86, 641–647.PubMedCrossRefGoogle Scholar
  42. Nielsen, R., Yang, Z., 1998. Likelihood models for detecting positively selected amino acid sites and applications tothe HIV-1 envelopegene. Genetics 148, 929–936.PubMedPubMedCentralGoogle Scholar
  43. Oliver, M.K., Telfer, S., Piertney, S.B., 2009. Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the watervole (Arvicola terrestris). Proc. R. Soc. B 276, 1119–1128.PubMedCrossRefGoogle Scholar
  44. Ortega, J., Arita, H., 1999. Structure and social dynamics of harem groups in Artibeus jamaicensis (Chiroptera: Phyllostomidae).J. Mammal 80, 1173–1185.CrossRefGoogle Scholar
  45. Ortega, J., Castro-Arellano, I., 2001. Artibeus jamaicensis. Mamm. Species 662, 1–9.CrossRefGoogle Scholar
  46. Ortega, J., Maldonado, E., Arita, H., Wilkinson, G., Fleischer, R., 2002. Characterization of microsatellite loci in theJamaican fruit-eating bat Artibeus jamaicensis and cross-species amplification. Mol. Ecol. Notes 2, 462–464.CrossRefGoogle Scholar
  47. Penn, D.J., Potts, W.K., 1999. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat 153, 145–163.PubMedCrossRefGoogle Scholar
  48. Piertney, S.B., Oliver, M.K., 2006. The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7–21.PubMedCrossRefGoogle Scholar
  49. Pond, S.L.K., Frost, S.D.W., 2005. Not sodifferent after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol 22, 1208–1222.CrossRefGoogle Scholar
  50. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  51. Raymond, M., Rousset, F., 1995. GenePop v1.2: population genetics software for exact test and ecumenicism. J. Hered 86, 248–249.CrossRefGoogle Scholar
  52. Richman, A., Herrera, L., Ortega-García, S., Flores-Martínez, J., Arroyo-Cabrales, J., Morales-Malacara, J., 2010. Class II DRB polymorphism and sequence diversity in two vesperbats in the genus Myotis. Immunogenetics 37, 401–405.CrossRefGoogle Scholar
  53. Rousset, F., 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour 8, 103–106.PubMedCrossRefGoogle Scholar
  54. Ruiz, E.A., Vargas-Miranda, B., Zúñiga, G., 2013. Late-pleistocene phylogeography and demographic history of two evolutionary lineages of Artibeus jamaicensis (Chiroptera: Phyllostomidae) in Mexico. Acta Chiropr 15, 19–33.CrossRefGoogle Scholar
  55. Schad, J., Dechmann, D.K.N., Voigt, C.C., Sommer, S., 2011. MHC class IIDRB diversity, selection pattern and population structure in Neotropical bat species, Noctilio albiventris. Heredity 107, 115–126.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Schad, J., Voigt, C.C., Greiner, S., Dechmann, D.K.N., Sommer, S., 2012. Independent evolution of functional MHC class II DRB genes in New World bat species. Immunogenetics 64, 535–547.PubMedCrossRefGoogle Scholar
  57. Schierup, M.H., Vekemans, X., Charlesworth, D., 2000. The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet. Resour 76, 51–62.CrossRefGoogle Scholar
  58. Schwensow, N., Fietz, J., Dausmann, K., Sommer, S., 2007. Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99, 265–277.PubMedCrossRefGoogle Scholar
  59. Seifertová, M., Simková, A., 2011. Structure, diversity and evolution patterns of expressed MHC class II B genes in chub (Squalius cephalus): a cyprinid fish species from Europe. Immunogenetics 63, 167–181.PubMedCrossRefGoogle Scholar
  60. Sikes, R.S., The Animal Care Use Committee of the American Society of Mammalogists, 2016. Guidelines of the American Society of Mammalogists for the use ofwild mammals in research and education. J. Mammal 97, 663–688.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Spurgin, L.G., Richardson, D.S., 2010. How pathogens drive genetic diversity MHC, mechanisms, and misunderstanding. Proc. R. Soc 277, 979–988.CrossRefGoogle Scholar
  62. Suzuki, Y., Gojobori, T., 1999. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol 16, 1315–1328.PubMedCrossRefGoogle Scholar
  63. Suzuki, Y., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T., Ohsumi, Y., 2001. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBOJ 20, 5971–5981.CrossRefGoogle Scholar
  64. Takahata, N., Nei, M., 1990. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124, 967–978.PubMedPubMedCentralGoogle Scholar
  65. Thomsen, M., Lundegaard, C., Buus, S., Lund, O., Nielsen, M., 2013. MHCcluster, a method for functional clustering of MHC molecules. Immunogenetics 65, 655–665.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Wakeland, E.K., Boehme, S., She, J.X., 1990. The generation and maintenance of MHC class II gene polymorphism in rodents. Immunol. Rev 113, 207–226.PubMedCrossRefGoogle Scholar
  67. Westerdahl, H., Hansson, B., Bensch, S., Hasselquist, D., 2004. Between year variation of MHC allele frequencies ingreat reed warblers: selection or drift.J. Evol. Biol 17, 485–492.CrossRefGoogle Scholar
  68. Worthington-Wilmer, J., Hall, L., Barrat, E., Moritz, C., 1999. Genetic structure and male-mediated gene flow in the ghost bat (Macroderma gigas). Evolution 53, 1583–1591.PubMedGoogle Scholar
  69. Yeager, M., Hughes, A.L., 1999. Evolution of mammalian MHC: natural selection, recombination, and convergent evolution. Immunol. Rev 167, 45–58.PubMedCrossRefGoogle Scholar
  70. Yeh, F.C., Yang, R.C., Boyle, T.B.J., Ye, Z., Mao, J.X., 1999. POPGENE Version 1.32, the User-friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada.Google Scholar
  71. Zhai, W., Nielsen, R., Slatkin, M., 2008. An investigation of statistical power of neutrality tests based on comparative and population genetic data. Mol. Biol. Evol 26, 273–283.PubMedPubMedCentralCrossRefGoogle Scholar
  72. van Oosterhout, C., Hutchinson, W.F., Willis, 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
  73. van Oosterhout, C., 2009. Transposons in the MHC: the Yin and Yang of the vertebrate immune system. Heredity 103, 190–191.PubMedCrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde, e. V. DGS 2017

Authors and Affiliations

  1. 1.Laboratorio de Biodiversidad, Unidad Académica de Ciencias BiológicasUniversidad Autónoma de ZacatecasZacatecasMéxico
  2. 2.Laboratorio de Bioconservación y Manejo, Posgrado en Ciencias Quimicobiológicas, Departamento de Zoología, Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalCiudad de MéxicoMéxico

Personalised recommendations