Can extreme MHC class I diversity be a feature of a wide geographic range? The example of Seba’s short-tailed bat (Carollia perspicillata)

  • Tamar Qurkhuli
  • Nina Schwensow
  • Stefan Dominik Brändel
  • Marco Tschapka
  • Simone SommerEmail author
Original Article


The major histocompatibility complex (MHC) is one of the most diverse genetic regions under pathogen-driven selection because of its central role in antigen binding and immunity. The highest MHC variability, both in terms of the number of individual alleles and gene copies, has so far been found in passerine birds; this is probably attributable to passerine adaptation to both a wide geographic range and a diverse array of habitats. If extraordinary high MHC variation and duplication rates are adaptive features under selection during the evolution of ecologically and taxonomically diverse species, then similarly diverse MHC architectures should be found in bats. Bats are an extremely species-rich mammalian group that is globally widely distributed. Many bat species roost in multitudinous groups and have high contact rates with pathogens, conspecifics, and allospecifics. We have characterized the MHC class I diversity in 116 Panamanian Seba’s short-tailed bats (Carollia perspicillata), a widely distributed, generalist, neotropical species. We have detected a remarkable individual and population-level diversity of MHC class I genes, with between seven and 22 alleles and a unique genotype in each individual. This diversity is comparable with that reported in passerine birds and, in both taxonomic groups, further variability has evolved through length polymorphisms. Our findings support the hypothesis that, for species with a geographically broader range, high MHC class I variability is particularly adaptive. Investigation of the details of the underlying adaptive processes and the role of the high MHC diversity in pathogen resistance are important next steps for a better understanding of the role of bats in viral evolution and as carriers of several deadly zoonotic viruses.


MHC I exon 2 diversity Copy number variation Length polymorphism Bat Carollia perspicillata Panama 



We thank the Smithsonian Tropical Research Institute in Panamá for providing the essential infrastructure and, especially, Oris Acevedo and Belkys Jimenéz for their constant help during our fieldwork. We are grateful to Rachel Page for all her support in realizing this project. We extend our thanks to all field assistants, to Kerstin Wilhelm and Ulrike Stehle for excellent technical assistance, and to Pablo Santos and all team members of the Sommer lab for fruitful discussions. We are also grateful to Theresa Jones for language editing.

Funding information

This research was funded by the German Science Foundation (DFG) and is part of the DFG Priority Program SPP 1596/2 Ecology and species barriers in emerging infectious diseases (SO 428/ 9-1, 9-2; TS 81/7-1, 7-2).

Supplementary material

251_2019_1128_MOESM1_ESM.docx (681 kb)
ESM 1 (DOCX 680 kb)
251_2019_1128_MOESM2_ESM.docx (39 kb)
ESM 2 (DOCX 38 kb)
251_2019_1128_MOESM3_ESM.docx (73 kb)
ESM 3 (DOCX 72 kb)
251_2019_1128_MOESM4_ESM.docx (16 kb)
ESM 4 (DOCX 16 kb)
251_2019_1128_MOESM5_ESM.xlsx (91 kb)
ESM 5 (XLSX 91 kb)
251_2019_1128_MOESM6_ESM.docx (15 kb)
ESM 6 (DOCX 15 kb)
251_2019_1128_MOESM7_ESM.docx (16 kb)
ESM 7 (DOCX 16 kb)


  1. Abduriyim S, Zou D-H, Zhao H (2019) Origin and evolution of the major histocompatibility complex class I region in eutherian mammals. Ecol Evol 9(13):7861–7874. CrossRefGoogle Scholar
  2. Adams EJ, Luoma AM (2013) The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I–like molecules. Annu Rev Immunol 31(1):529–561. CrossRefGoogle Scholar
  3. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci 101:3490–3494. CrossRefGoogle Scholar
  4. Alcaide M, Edwards SV, Negro JJ et al (2008) Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665. CrossRefGoogle Scholar
  5. Alcaide M, Liu M, Edwards SV (2013) Major histocompatibility complex class I evolution in songbirds: universal primers, rapid evolution and base compositional shifts in exon 3. PeerJ 1:e86. CrossRefGoogle Scholar
  6. Alcaide M, Muñoz J, la Puente JM et al (2014) Extraordinary MHC class II B diversity in a non-passerine, wild bird: the Eurasian coot Fulica atra (Aves: Rallidae). Ecol Evol 4:688–698. CrossRefGoogle Scholar
  7. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. CrossRefGoogle Scholar
  8. Anthony SJ, Ojeda-Flores R, Rico-Chavez O, Navarrete-Macias I, Zambrana-Torrelio CM, Rostal MK, Epstein JH, Tipps T, Liang E, Sanchez-Leon M, Sotomayor-Bonilla J, Aguirre AA, Avila-Flores R, Medellin RA, Goldstein T, Suzan G, Daszak P, Lipkin WI (2013) Coronaviruses in bats from Mexico. J Gen Virol 94:1028–1038. CrossRefGoogle Scholar
  9. Anzai T, Shiina T, Kimura N, Yanagiya K, Kohara S, Shigenari A, Yamagata T, Kulski JK, Naruse TK, Fujimori Y, Fukuzumi Y, Yamazaki M, Tashiro H, Iwamoto C, Umehara Y, Imanishi T, Meyer A, Ikeo K, Gojobori T, Bahram S, Inoko H (2003) Comparative sequencing of human and chimpanzee MHC class I regions unveils insertions/deletions as the major path to genomic divergence. Proc Natl Acad Sci 100:7708–7713. CrossRefGoogle Scholar
  10. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224. CrossRefGoogle Scholar
  11. Baker ML, Schountz T, Wang L-F (2013) Antiviral immune responses of bats: a review. Zoonoses Public Health 60:104–116. CrossRefGoogle Scholar
  12. Balasubramaniam S, Mulder RA, Sunnucks P, Pavlova A, Melville J (2017) MHC class II β exon 2 variation in pardalotes (Pardalotidae) is shaped by selection, recombination and gene conversion. Immunogenetics 69:101–111. CrossRefGoogle Scholar
  13. Banerjee A, Kulcsar K, Misra V, Frieman M, Mossman K (2019) Bats and coronaviruses. Viruses 11:41. CrossRefGoogle Scholar
  14. Barquez R, Perez S, Miller B, Diaz M (2015) Carollia perspicillata. The IUCN red list of threatened species 2015: e.T3905A22133716. Downloaded on 21 June 2019
  15. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377. CrossRefGoogle Scholar
  16. Biedrzycka A, O’Connor E, Sebastian A, Migalska M, Radwan J, Zając T, Bielański W, Solarz W, Ćmiel A, Westerdahl H (2017) Extreme MHC class I diversity in the sedge warbler (Acrocephalus schoenobaenus); selection patterns and allelic divergence suggest that different genes have different functions. BMC Evol Biol 17:159. CrossRefGoogle Scholar
  17. Bjorkman PJ, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59:253–288. CrossRefGoogle Scholar
  18. Bonhomme M, Doxiadis GG, Heijmans CM et al (2008) Genomic plasticity of the immune-related Mhc class I B region in macaque species. BMC Genomics 9:514. CrossRefGoogle Scholar
  19. Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047. CrossRefGoogle Scholar
  20. Bonneaud C, Sorci G, Morin V et al (2004) Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 55:855–865. CrossRefGoogle Scholar
  21. Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265. CrossRefGoogle Scholar
  22. Carrington CVF, Foster JE, Zhu HC, Zhang JX, Smith GJD, Thompson N, Auguste AJ, Ramkissoon V, Adesiyun AA, Guan Y (2008) Detection and phylogenetic analysis of group 1 coronaviruses in south American bats. Emerg Infect Dis 14:1890–1893. CrossRefGoogle Scholar
  23. Chu DKW, Poon LLM, Guan Y, Peiris JSM (2008) Novel Astroviruses in insectivorous bats. J Virol 82:9107–9114. CrossRefGoogle Scholar
  24. Corman VM, Rasche A, Diallo TD, Cottontail VM, Stocker A, Souza BFCD, Correa JI, Carneiro AJB, Franke CR, Nagy M, Metz M, Knornschild M, Kalko EKV, Ghanem SJ, Morales KDS, Salsamendi E, Spinola M, Herrler G, Voigt CC, Tschapka M, Drosten C, Drexler JF (2013) Highly diversified coronaviruses in neotropical bats. J Gen Virol 94:1984–1994. CrossRefGoogle Scholar
  25. D’Souza MP, Adams E, Altman JD, Birnbaum ME, Boggiano C, Casorati G, Chien YH, Conley A, Eckle SBG, Früh K, Gondré-Lewis T, Hassan N, Huang H, Jayashankar L, Kasmar AG, Kunwar N, Lavelle J, Lewinsohn DM, Moody B, Picker L, Ramachandra L, Shastri N, Parham P, McMichael AJ, Yewdell JW (2019) Casting a wider net: Immunosurveillance by nonclassical MHC molecules. PLoS Pathog 15(2):e1007567. CrossRefGoogle Scholar
  26. de Groot NG, Heijmans CMC, van der Wiel MKH, Blokhuis JH, Mulder A, Guethlein LA, Doxiadis GGM, Claas FHJ, Parham P, Bontrop RE (2016) Complex MHC class I gene transcription profiles and their functional impact in orangutans. J Immunol 196:750–758. CrossRefGoogle Scholar
  27. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. CrossRefGoogle Scholar
  28. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S (2005) Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci 102:7922–7927. CrossRefGoogle Scholar
  29. Donato C, Vijaykrishna D (2017) The broad host range and genetic diversity of mammalian and avian Astroviruses. Viruses 9:102. CrossRefGoogle Scholar
  30. Doxiadis GGM, Rouweler AJM, de Groot NG, Louwerse A, Otting N, Verschoor EJ, Bontrop RE (2006) Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques. Immunogenetics 58:259–268. CrossRefGoogle Scholar
  31. Drews A, Strandh M, Råberg L, Westerdahl H (2017) Expression and phylogenetic analyses reveal paralogous lineages of putatively classical and non-classical MHC-I genes in three sparrow species (Passer). BMC Evol Biol 17(1):152. CrossRefGoogle Scholar
  32. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. CrossRefGoogle Scholar
  33. Eirín-López JM, Rebordinos L, Rooney AP, Rozas J (2012) The birth-and-death evolution of multigene families revisited. Repetitive DNA 7:170–196. CrossRefGoogle Scholar
  34. Eren AM, Maignien L, Sul WJ, Murphy LG, Grim SL, Morrison HG, Sogin ML (2013) Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol Evol 4:1111–1119. CrossRefGoogle Scholar
  35. Fagrouch Z, Sarwari R, Lavergne A, Delaval M, de Thoisy B, Lacoste V, Verschoor EJ (2012) Novel polyomaviruses in south American bats and their relationship to other members of the family Polyomaviridae. J Gen Virol 93:2652–2657. CrossRefGoogle Scholar
  36. Fenton MB, Simmons NB (2015) Bats: a world of science and mystery. University of Chicago PressGoogle Scholar
  37. Fischer Lindahl K, Byers DE, Dabhi VM, Hovik R, Jones EP, Smith GP, Wang CR, Xiao H, Yoshino M (1997) H2-M3, a full-service class Ib histocompatibility antigen. Annu Rev Immunol 15(1):851–879. CrossRefGoogle Scholar
  38. Fischer K, Pinho dos Reis V, Balkema-Buschmann A (2017) Bat Astroviruses: towards understanding the transmission dynamics of a neglected virus family. Viruses 9:34. CrossRefGoogle Scholar
  39. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582. CrossRefGoogle Scholar
  40. Gillingham MAF, Bechet A, Courtiol A, Rendón-Martos M, Amat JA, Samraoui OO, Sommer S, Cezilly F (2017) Very high MHC class IIB diversity without spatial differentiation in the Mediterranean population of greater flamingos. BMC Evol Biol 17(1):56CrossRefGoogle Scholar
  41. Gillingham MAF, Montero BK, Wilhelm K, Grudzus K, Sommer S, Santos PSC (2019) A novel workflow to improve multi-locus genotyping of wildlife species: an experimental set-up with a known model system. bioRxiv:638288.
  42. Gordon A, Hannon GJ (2010) Fastx-toolkit: FASTQ/a short-reads preprocessing toolsGoogle Scholar
  43. Hansen SG, Wu HL, Burwitz BJ, Hughes CM, Hammond KB, Ventura AB, Reed JS, Gilbride RM, Ainslie E, Morrow DW, Ford JC, Selseth AN, Pathak R, Malouli D, Legasse AW, Axthelm MK, Nelson JA, Gillespie GM, Walters LC, Brackenridge S, Sharpe HR, Lopez CA, Fruh K, Korber BT, McMichael AJ, Gnanakaran S, Sacha JB, Picker LJ (2016) Broadly targeted CD8+ T cell responses restricted by major histocompatibility complex E. Science 351(6274):714–720. CrossRefGoogle Scholar
  44. Holmes EC, Worobey M, Rambaut A (1999) Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 16:405–409. CrossRefGoogle Scholar
  45. Hosomichi K, Miller MM, Goto RM, Wang Y, Suzuki S, Kulski JK, Nishibori M, Inoko H, Hanzawa K, Shiina T (2008) Contribution of mutation, recombination, and gene conversion to chicken Mhc-B haplotype diversity. J Immunol 181:3393–3399. CrossRefGoogle Scholar
  46. Huchard E, Knapp LA, Wang J et al (2010) MHC, mate choice and heterozygote advantage in a wild social primate. Mol Ecol 19:2545–2561. Google Scholar
  47. Hughes AL, Yeager M (1997) Comparative evolutionary rates of introns and exons in murine rodents. J Mol Evol 45:125–130. CrossRefGoogle Scholar
  48. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. CrossRefGoogle Scholar
  49. Kaufman J (2018) Unfinished business: evolution of the MHC and the adaptive immune system of jawed vertebrates. Annu Rev Immunol 36:383–409. CrossRefGoogle Scholar
  50. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. CrossRefGoogle Scholar
  51. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695. CrossRefGoogle Scholar
  52. Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276. CrossRefGoogle Scholar
  53. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University PressGoogle Scholar
  54. Klein J (1986) Natural history of the major histocompatibility complex. WileyGoogle Scholar
  55. Klein J, Kasahara M, Gutknecht J, Figueroa F (1990) Origin and function of Mhc polymorphism. 1939-1989 Fifty Years Prog Allergy 49:35–50.
  56. Klitz W, Hedrick P, Louis EJ (2012) New reservoirs of HLA alleles: pools of rare variants enhance immune defense. Trends Genet 28:480–486. CrossRefGoogle Scholar
  57. Kosakovsky Pond SL, Frost SDW (2005a) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533. CrossRefGoogle Scholar
  58. Kosakovsky Pond SL, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222. CrossRefGoogle Scholar
  59. Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. CrossRefGoogle Scholar
  60. Luis AD, Hayman DTS, O’Shea TJ et al (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc R Soc B 280:20122753. CrossRefGoogle Scholar
  61. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. CrossRefGoogle Scholar
  62. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563. CrossRefGoogle Scholar
  63. Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified Bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retrovir 21:98–102. CrossRefGoogle Scholar
  64. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1.
  65. 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. CrossRefGoogle Scholar
  66. Minias P, Pikus E, Whittingham LA, Dunn PO (2018) A global analysis of selection at the avian MHC. Evolution 72:1278–1293. CrossRefGoogle Scholar
  67. Miska KB, Harrison GA, Hellman L, Miller RD (2002) The major histocompatibility complex in monotremes: an analysis of the evolution of Mhc class I genes across all three mammalian subclasses. Immunogenetics 54:381–393. CrossRefGoogle Scholar
  68. Moratelli R, Calisher CH (2015) Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses? Mem Inst Oswaldo Cruz 110:1–22. CrossRefGoogle Scholar
  69. Murphy K, Weaver C (2017) Janeway’s immunobiology. Garland ScienceGoogle Scholar
  70. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764. CrossRefGoogle Scholar
  71. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205. CrossRefGoogle Scholar
  72. Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci 94:7799–7806. CrossRefGoogle Scholar
  73. Ng JHJ, Tachedjian M, Deakin J, Wynne JW, Cui J, Haring V, Broz I, Chen H, Belov K, Wang LF, Baker ML (2016) Evolution and comparative analysis of the bat MHC-I region. Sci Rep 6:21256. CrossRefGoogle Scholar
  74. Nicholls JA, Double MC, Rowell DM, Magrath RD (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176. CrossRefGoogle Scholar
  75. Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P (2017) Host and viral traits predict zoonotic spillover from mammals. Nature 546:646–650. CrossRefGoogle Scholar
  76. Otting N, Heijmans CMC, Noort RC, de Groot NG, Doxiadis GGM, van Rood JJ, Watkins DI, Bontrop RE (2005) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci 102:1626–1631. CrossRefGoogle Scholar
  77. Papenfuss AT, Baker ML, Feng Z-P, Tachedjian M, Crameri G, Cowled C, Ng J, Janardhana V, Field HE, Wang LF (2012) The immune gene repertoire of an important viral reservoir, the Australian black flying fox. BMC Genomics 13:261. CrossRefGoogle Scholar
  78. Pavlovich SS, Lovett SP, Koroleva G et al (2018) The Egyptian rousette genome reveals unexpected features of bat antiviral immunity. Cell 173:1098–1110.e18. CrossRefGoogle Scholar
  79. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci 98:13757–13762. CrossRefGoogle Scholar
  80. Prugnolle F, Manica A, Charpentier M, Guégan JF, Guernier V, Balloux F (2005) Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol 15:1022–1027. CrossRefGoogle Scholar
  81. Real-Monroy MD, Martínez-Méndez N, Ortega J (2014) MHC-DRB exon 2 diversity of the Jamaican fruit-eating bat (Artibeus jamaicensis) from Mexico. Acta Chiropterol 16:301–314. CrossRefGoogle Scholar
  82. Reusch TB, Schaschl H, Wegner KM (2004) Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56:427–437CrossRefGoogle Scholar
  83. Richman AD, Herrera MLG, Ortega-García S et al (2010) Class II DRB polymorphism and sequence diversity in two vesper bats in the genus Myotis. Int J Immunogenet 37:401–405. CrossRefGoogle Scholar
  84. Robinson J, Malik A, Parham P, Bodmer JG, Marsh SGE (2000) IMGT/HLA database–a sequence database for the human major histocompatibility complex. Tissue Antigens 55:280–287CrossRefGoogle Scholar
  85. Rock KL, Reits E, Neefjes J (2016) Present yourself! By MHC class I and MHC class II molecules. Trends Immunol 37:724–737. CrossRefGoogle Scholar
  86. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics methods and protocols. Springer, pp 365–386Google Scholar
  87. Salmier A, de Thoisy B, Crouau-Roy B, Lacoste V, Lavergne A (2016) Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species. BMC Evol Biol 16:229. CrossRefGoogle Scholar
  88. Salmón-Mulanovich G, Vásquez A, Albújar C, Guevara C V, Laguna-Torres A, Salazar M, Zamalloa H, Cáceres M, Gómez-Benavides J, Pacheco V, Contreras C, Kochel T, Niezgoda M, Jackson FR, Velasco-Villa A, Rupprecht C, Montgomery JM (2009) Human rabies and rabies in vampire and nonvampire bat species, southeastern Peru, 2007. Emerg Infect Dis 15:1308–1311. CrossRefGoogle Scholar
  89. Santos PSC, Courtiol A, Heidel AJ, Höner OP, Heckmann I, Nagy M, Mayer F, Platzer M, Voigt CC, Sommer S (2016) MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal. Sci Rep 6:38490. CrossRefGoogle Scholar
  90. Santos PSC, Mezger M, Kolar M, Michler FU, Sommer S (2018) The best smellers make the best choosers: mate choice is affected by female chemosensory receptor gene diversity in a mammal. Proc R Soc B Biol Sci 285:20182426. CrossRefGoogle Scholar
  91. Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis. St LouisGoogle Scholar
  92. Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2019) GenBank. Nucleic Acids Res 47:D94–D99. CrossRefGoogle Scholar
  93. Schad J, Dechmann DK, Voigt CC, Sommer S (2011) MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris. Heredity 107:115–126CrossRefGoogle Scholar
  94. Schad J, Dechmann DKN, Voigt CC, Sommer S (2012a) Evidence for the ‘good genes’ model: association of MHC class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris. PLoS One 7:e37101. CrossRefGoogle Scholar
  95. Schad J, Voigt CC, Greiner S, Dechmann DKN, Sommer S (2012b) Independent evolution of functional MHC class II DRB genes in New World bat species. Immunogenetics 64:535–547. CrossRefGoogle Scholar
  96. Schaschl H, Tobler M, Plath M et al (2008) Polymorphic MHC loci in an asexual fish, the amazon molly (Poecilia formosa; Poeciliidae). Mol Ecol 17:5220–5230. CrossRefGoogle Scholar
  97. Schmid J, Rasche A, Eibner G, Jeworowski L, Page RA, Corman VM, Drosten C, Sommer S (2018) Ecological drivers of Hepacivirus infection in a Neotropical rodent inhabiting landscapes with various degrees of human environmental change. Oecologia 188(1):289–302CrossRefGoogle Scholar
  98. Schwensow N, Castro-Prieto A, Wachter B, Sommer S (2019) Immunological MHC supertypes and allelic expression: how low is the functional MHC diversity in free-ranging Namibian cheetahs? Conserv Genet 20:65–80. CrossRefGoogle Scholar
  99. Siddle HV, Marzec J, Cheng Y, Jones M, Belov K (2010) MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. Proc R Soc Lond B Biol Sci 277:2001–2006. CrossRefGoogle Scholar
  100. Simmons NB (2005) Order Chiroptera pp. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp 312–529Google Scholar
  101. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129. Google Scholar
  102. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16. CrossRefGoogle Scholar
  103. Sommer S, Courtiol A, Mazzoni CJ (2013) MHC genotyping of non-model organisms using next-generation sequencing: a new methodology to deal with artefacts and allelic dropout. BMC Genomics 14:542. CrossRefGoogle Scholar
  104. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B 277:979–988. CrossRefGoogle Scholar
  105. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. CrossRefGoogle Scholar
  106. Teeling EC, Springer MS, Madsen O, Bates P, O'brien S, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584. CrossRefGoogle Scholar
  107. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. CrossRefGoogle Scholar
  108. van der Wiel MKH, Doxiadis GGM, de Groot N, Otting N, de Groot NG, Poirier N, Blancho G, Bontrop RE (2018) MHC class I diversity of olive baboons (Papio anubis) unravelled by next-generation sequencing. Immunogenetics 70:439–448. CrossRefGoogle Scholar
  109. Wasimuddin, Brändel SD, Tschapka M et al (2018) Astrovirus infections induce age-dependent dysbiosis in gut microbiomes of bats. ISME J 12:2883–2893. CrossRefGoogle Scholar
  110. Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Royal Society of London. Proceedings B. Biol Sci 272(1571):1511–1518.
  111. Wynne JW, Woon AP, Dudek NL, Croft NP, Ng JHJ, Baker ML, Wang L-F, Purcell AW (2016) Characterization of the antigen processing machinery and endogenous peptide presentation of a bat MHC class I molecule. J Immunol 196(11):4468–4476.
  112. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. CrossRefGoogle Scholar
  113. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute for Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  2. 2.Smithsonian Tropical Research InstitutePanamáRepública de Panamá

Personalised recommendations