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

Volumn 7, Issue 5, 2012, Pages

  Schad, Julia ^a   Dechmann, Dina K N ^b,c   Voigt, Christian C ^a   Sommer, Simone ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ARTICLE; BAT; BODY SIZE; CONTROLLED STUDY; DNA ISOLATION; DRB GENE; ECTOPARASITE; ECTOPARASITISM; FEMALE; GENE; GENE FREQUENCY; GENETIC MODEL; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HETEROZYGOSITY; INFESTATION; MALE; NOCTILIO ALBIVENTRIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITISM; PROTEIN ANALYSIS;

ALLELES; ANIMALS; CHIROPTERA; DIPTERA; DISEASE RESISTANCE; GENE FREQUENCY; GENES, MHC CLASS II; GENETIC VARIATION; GENOTYPE; MALE; REPRODUCTION; TICK INFESTATIONS; TICKS;

IXODIDA; NOCTILIO ALBIVENTRIS; STREBLIDAE;

EID: 84861215246     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037101     Document Type: Article

References (87)

1. Sheldon BC, Verhulst S, (1996) Ecological immunology: costly parasite defence and trade-offs in evolutionary ecology. Trends in Ecol Evol 11: 317-321.
2. Lochmiller RL, Deerenberg C, (2000) Trade-offs in evolutionary Immunology: just what is he cost of immunity? Oikos 88: 87-98.
3. Zuk M, Stoehr AM, (2002) Immune defence and host life history. Am Nat 160: S9-S22.
4. Folstad I, Karter AJ, (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 129: 603-622.
5. Knowles SCL, Nakagawa S, Sheldon BC, (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Funct Ecol 23: 405-415.
6. McCallum ML, Trauth S, (2007) Physiological Trade-offs between immunity and reproduction in the northern cricket frog (Acris crepitans). Herpetologica 63 (3): 269-274.
7. Boonekamp JJ, Ros AHF, Verhulst S, (2008) Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Letters 4: 741-744.
8. Greiner S, Stefanski V, Dehnhardt M, Voigt CC, (2010) Plasma testosterone levels decrease after activation of skin immune system in a free-ranging mammal. Gen Comp Endocrinol 168: 466-473.
9. Hamilton WD, Zuk M, (1982) Heritable true fitness and bright birds: A role for parasites? Science 218: 384-387.
10. Piertney SB, Oliver MK, (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
11. Klein J, (1986) Natural history of the major histocompatibility complex. Wiley & Sons, New York.
12. 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.
13. Sommer S, (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2: 16.
14. Wikel SK, (1996) Host immunity to ticks. Annu Rev Entomol 41: 1-22.
15. Andrade BB, Teixeira CR, Barral A, Barral-Netto M, (2005) Haematophagous arthropod saliva and host defence system: a tale of tear and blood. An Acad Bras Cience 77 (4): 665-693.
16. Milleron RS, Ribeiro JMC, Elnaime D, Soong L, Lanzaro GZ, (2004) Negative effect on antibodies against maxadilan on the fitness of the sand fly vector of American visceral Leishmaniasis. A, J Trop Med Hyg 70: 286-293.
17. Wikel SK, (1999) Tick modulation of host immunity: an important factor in pathogen transmission. Annu Rev Entomol 41: 1-22.
18. Schoeler GB, Wikel SK, (2001) Modulation of host immunity by haematophagus arthropods. Ann Trop Med Parasitol 95 (8): 755-771.
19. Francischetti IMB, Sá-Numes A, Mans BJ, Santos IM, Ribeiro JMC, (2009) The role of saliva in tick feeding. Front Biosci 14: 2051-2088.
20. Alexander JO'D, (1986) The physiology of itch. Parasitol Today 2: 345-51.
21. Giorgi MS, Arlettaz R, Christe P, Vogel P, (2001) The energetic grooming costs imposed by a parasitic mite (Sinturnix myoti). Proc R Soc Lond B Biol Sci 268: 2071-2075.
22. Marshall AG, Ecology of Bats Kunze TH (ed) (1982) Ecology of insects ectoparasitic on bats. pp. 369-399 Plenum Publishing Corporation, New York, Lond.
23. Møller AP, (1993) Ectoparasites increase the cost of reproduction in their host. J Anim Ecol 62: 309-322.
24. Christe P, Arlettaz R, Vogel P, (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3: 307-212.
25. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, et al. (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Ann Rev Ecol Evol Syst 34: 517-547.
26. Krasnov BR, Shenbrot GI, Khoklova IS, Poulin R, (2005) Diversification of ectoparasite assemblages and climate: an example with fleas parasitic on small mammals. Global Ecol Biogeogr 14: 167-175.
27. Presley SJ, Willig MR, (2008) Intraspecific patterns of ectoparasites abundances on Paraguayan bats: effects of host sex and body size. J Trop Ecol 24: 75-83.
28. Patterson BD, Dick CW, Dittmar K, (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23: 177-189.
29. Giorgi MS, Arlettaz R, Guillaume F, Nusslé S, Ossola C, et al. (2004) Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138: 648-654.
30. Dick CW, Patterson BD, (2007) Against all odds: Explaining high host specificity in dispersal-prone parasites. Int J Parasitol 37: 871-876.
31. Schad J, Dechmann DKN, Voigt CC, Sommer S, (2011) MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris. Heredity 107: 115-126.
32. Hood CS, Pitocchelli J, (1983) Noctilio albiventris. Mammalian Species 197: 1-5.
33. Krutzsch PH, (2000) Anatomy, physiology and cyclicity of the male reproductive tract. In: Krutzsch TH, Crichton EG, editors. Reproductive biology of bats pp. 91-156 Academic Press, London.
34. Brunet-Rossini AK, Wilkinson GS, (2009) Methods for age estimation and the study of senescence in bats. In: Kunz TH, editors. Ecological and behavioural methods for the study of bats Smithsonian Institution, Washington, DC, second edition, chapter 15.
35. Racey PA, (2009) Reproductive assessment of bats. In: Kunz TH, editors. Ecological and behavioural methods for the study of bats Smithsonian Institution, Washington, DC, second edition, chapter 12.
36. Studier EH, Lavoie KH, (1984) Microbial involvement in scent production in noctilionid bats. J Mammal 65: 711-714.
37. Heusner AA, (1985) Body size and energy metabolism. Annu Rev Nutr 5: 267-293.
38. Glazier DS, (2005) Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev 80: 611-662.
39. Presley, (2007) Streblid bat fly assemblage structure on Paraguayan Noctilio leporinus (Chiroptera: Noctilionidae): nestedness and species co-occurrence, J Trop Ecol 23: 409-417.
40. Worthington-Wilmer J, Baratt E, (1996) A non-lethal method of tissue-sampling for genetic studies of chiropterans. Bat Research News 37: 1-3.
41. Wenzel RL, Tipton VJ, (1966) Ectoparasites of Panama. Field Museum of Natural History, Chicago.
42. Wenzel RL, (1976) The streblid bat flies of Venezuela (Diptera: Streblidae). Brig Young Univ Sci Bull 20: 1-77.
43. Dick CW, Miller JA, (2010) Streblidae. In: Brown BV, Wood M, Borkent A, editors. Manual of Central American Diptera (Vol II) pp. 1249-1260 National Research Council Press, Ottawa.
44. 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.
45. Hedrick P, (2005) A standardized genetic differentiation measure. Evolution 59: 1633-1638.
46. Joost L, (2008) GST and its relatives do not measure differentiation. Mol Ecol 17: 4015-4026.
47. Crawford NG, (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Res 10: 556-557.
48. Faul F, Erdfelder E, (1992) GPOWER: A priori, post-hoc, and compromise power analyses for MS-Dos (Computer program) Bonn, FRG Bonn University Dep. Psychology.
49. Cohen J, (1988) Statistical power analyses for the behavioural science (2nd ed.) Hilsdale, NJ Lawrence Earlbaum Associates.
50. O'Hara RB, Kotze JD, (2010) Do not log-transform count data. Meth Ecol Evol 1: 118-122.
51. Zuur AF, Ieno EN, Elphick CS, (2010) A protocol for data exploration to avoid common statistical problems. Meth Ecol Evol 1: 3-14.
52. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM, (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY, USA.
53. Booth GD, Niccolucci MJ, Schuster EG, (1994) Identifying proxy sets in multiple linear regression: an aid to better coefficient interpretation. Intermountain Research Station, USDA Forest Service, Ogden, Utah, USA.
54. Pinheiro J, Bates D, (2000) Mixed effect models in S and S-Plus. Springer, New York, USA.
55. Bolker BM, Brooks ME, Clark CJ, Geange AW, Poulsen JR, et al. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24 (3): 127-135.
56. Fitzmaurice GN, Laird NM, Ware J, (2004) Applied longitudinal analysis. John Wiley & Sons, New York.
57. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
58. Presley SJ, (2004) Ectoparasitic assemblages of Paraguayan bats: ecological and evolutionary perspectives. PhD dissertation, Texas Tech University, Lubbock, Texas, USA.
59. ter Hofstede HM, Fenton MB, (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J Zool Lond 266: 333-340.
60. Pearce RD, O'Shea TJ, (2007) Ectoparasites in an urban population of big brown bats (Eptesicus fuscus) in Colorado. J Parasitol 93 (3): 518-530.
61. Mans BJ, (2011) Evolution of vertebrate hemostatic and inflammatory control mechanisms in blood-feeding arthropods. J Innate Immun 3: 41-51.
62. Rosenzweig ML, (1995) Species diversity in space and time. Cambridge University Press, Cambridge.
63. Christe P, Giorgi MS, Vogel P, Arlettaz R, (2003) Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? J Anim Ecol 72: 866-872.
64. Hawlena H, Abramsky Z, Krasnov BR, (2005) Age-biased parasitism and density-dependant distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 148: 30-39.
65. Poulin R, George-Nascimento M, (2007) The scaling of total parasite biomass with host body mass. Int J Parasitol 37: 359-364.
66. Moore SL, Wilson K, (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297: 2015-2018.
67. Christe P, Glaizot O, Evanno G, Bruyndonckx, Devevey G, et al. (2007) Host sex and ectoparasites choice: preference for, and higher survival on female hosts. J Anim Ecol 76: 703-710.
68. Patterson BD, Dick CW, Dittmar K, (2008) Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae). J Trop Ecol 24: 387-396.
69. Sharifi M, Mozafari F, Taghinezhad N, Javanbakht H, (2008) Variation in ectoparasite load reflects life history trades in the lesser mouse-eared bat, Myotis blythii (Chiroptera: Vespertilionidae) in Western Iran. J Parasitol 94 (3): 622-625.
70. Aluvia Y, Margalit H, (2004) A structure-based approach for prediction of MHC-binding peptides. Meth Bioinformatics in Vaccin Design 34: 454-459.
71. Goüy de Bellocq J, Charbonnel N, Morand S, (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Evol Biol 21: 1144-1150.
72. Poulin R, Morand S, (2004) Parasite biodiversity. Smithsonian Books.
73. Untalan PM, Pruett JH, Steelman CD, (2007) Association of the bovine leukocyte antigen major histocompatibility complex class II DRB*4401 allele with host resistance to the Lone Star tick, Amblyomma americanum. Vet Parasitol 145: 190-195.
74. Ditchkoff SS, Hoofer SR, Lochmiller L, Masters RE, Van den Busche RA, (2005) MHC-DRB evolution provides insight into parasite resistance in white-tailed deer. Southwest Nat 50 (1): 57-64.
75. Oliver MK, Telfer S, Piertney SB, (2009) Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proc R Soc B 267: 1119-1128.
76. Penn DJ, Potts WK, (1998) How do major histocompatibility complex genes influence odour and mating preference? Adv Immunol 69: 411-436.
77. Kwak J, Opiekun MC, Matsumura K, Preti G, Yamazaki K, et al. (2009) Major histocompatibility complex-regulated odortypes: Peptid-free urinary volatile signals. Phys Behav 96: 184-188.
78. Santos PSC, Kellermann T, Uchanska-Ziegler B, Ziegler A, (2010) Genomic architecture of MHC linked odorant receptor gene repertoires among 16 vertebrate species. Immunogenetics 62 (9): 569-584.
79. Krasnov BR, Khoklova IS, Oguzoglu I, Burdelova NI, (2002) Host discrimination by two desert fleas using an odour cue. Animal Behav 64: 33-40.
80. Lourenço S, Palmeirim JM, (2008) How do ectoparasittc nycteribiids locate their bat hosts? Parasitology 135: 1205-1213.
81. Logan JG, (2008) Why do mosquitoes "choose" to bite some people more than others? Outlooks on Pest Management pp. 280-283.
82. Verhulst NO, Qiu YT, Beijleveld H, Maliepaard C, Knights D, et al. (2011) Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLoS ONE 6 (12): e28991.
83. Penn DJ, Potts WK, (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153: 145-164.
84. Ilmonen P, Stundner G, Thoss M, Penn DJ, (2009) Females prefer the scent of outbred males: good-genes as heterozygosity? BMC Evol Biol 9: 104.
85. Doherty PC, Zinkernagel RM, (1975) Enhanced Immunological Surveillance in Mice Heterozygous at H-2 Gene Complex. Nature 256: 50-52.
86. Ditchkoff SS, Hoofer SR, Lochmiller L, Masters RE, Hoofer SR, et al. (2001) Major histocompatibility complex associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution 55: 616-625.
87. Milinski M, Griffiths SW, Reusch TBH, Boehm T, (2010) Costly major histocompatibility complex signals produced only by reproductively active males, but not females, must be validated by a 'maleness signal' in three-spined sticklebacks. Proc R Soc B 277: 391-398.