Major histocompatibility complex based resistance to a common bacterial pathogen of amphibians

PLoS ONE

Volumn 3, Issue 7, 2008, Pages

  Barribeau, Seth M ^a,b   Villinger, Jandouwe ^a,c   Waldman, Bruce ^a,d  

^a UNIVERSITY OF CANTERBURY   (New Zealand)

^b EMORY UNIVERSITY   (United States)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^d LINCOLN UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

AEROMONAS HYDROPHILA; ALLELE; AMPHIBIA; ARTICLE; BREEDING; CONTROLLED STUDY; GENETIC RESISTANCE; GENOTYPE; GROWTH RATE; HAPLOTYPE; HETEROZYGOTE; HOMOZYGOTE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; TADPOLE; XENOPUS LAEVIS; AEROMONAS; ANIMAL; BACTERIAL INFECTION; FEMALE; GENE EXPRESSION REGULATION; HEART; HUMAN; IMMUNE SYSTEM; INNATE IMMUNITY; MALE; METABOLISM; MICROBIOLOGY;

AEROMONAS HYDROPHILA; AMPHIBIA; BACTERIA (MICROORGANISMS); XENOPUS LAEVIS;

AEROMONAS; ALLELES; AMPHIBIA; ANIMALS; BACTERIAL INFECTIONS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HEART; HUMANS; IMMUNE SYSTEM; IMMUNITY, NATURAL; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; XENOPUS LAEVIS;

EID: 49949097321     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002692     Document Type: Article

References (81)

1. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256: 50-52.
2. McClelland EE, Penn D, Potts WK (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infect Immun 71: 2079-2086.
3. Penn D, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA 99:11260-11264.
4. Liu Y, Kasahara M, Rumfelt LL, Flajnik MF (2002) Xenopus class II A genes: studies of genetics, polymorphism, and expression. Dev Comp Immunol 26: 735-750.
5. Nonaka M, Namikawa C, Kato Y, Sasaki M, Salter-Cid L, et al. (1997) Major histocompatibility complex gene mapping in the amphibian Xenopus implies primordial organization. Proc Natl Acad Sci USA 94: 5789-5791.
6. Salter-Cid L, Nonaka M, FIajnik MF (1998) Expression of MHC class Ia and class Ib during ontogeny: high expression in epithelia and coregulation of class Ia and lmp7 genes. J Immunol 160: 2853-2861.
7. Flajnik MF, Hsu E, Kaufman JF, Du Pasquier L (1987) Changes in the immune system during metamorphosis of Xenopus. Immunol Today 8: 58--64.
8. Gantress J, Maniero GD, Cohen N, Robert J (2003) Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311: 254-262.
9. Waldman B, Tocher M (1998) Behavioral ecology, genetic diversity, and declining amphibian populations. In: Caro T, ed. Behavioral ecology and conservation biology. New York: Oxford University Press. pp 393-443.
10. Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23: 459-472.
11. Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404: 752-755.
12. Lips KR, Mendelson JR, Muñoz-Alonso A, Canseco-Marquez L, Mulcahy DG (2004) Amphibian population declines in montane southern Mexico: resurveys of historical localities. Biol Conserv 119: 555-564.
13. Mendelson JR III, Lips KR, Gagliardo RW, Rabb GB, Collins JP, et al. (2006) Confronting amphibian declines and extinctions. Science 313: 48.
14. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783-1786.
15. Edwards SV, Potts W (1996) Polymorphism of genes in the major histocompatibility complex (MHC): implications for conservation genetics of vertebrates. In: Smith TB, Wayne RK, eds. Molecular genetic approaches in conservation. New York: Oxford University Press. pp 214-237.
16. Hughes AL (1991) MHC polymorphism and the design of captive breeding programs. Conserv Biol 5: 249-251.
17. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95: 9031-9036.
18. Bosch J, Martínez-Solano I, García-París M (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol Conserv 97: 331-337.
19. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, et al. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci USA 103: 3165-3170.
20. Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, et al. (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87: 1671-1683.
21. Cunningham AA, Langton TES, Bennett PM, Lewin JF, Drury SEN, et al. (1996) Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philos Trans R Soc Lond B 351: 1539-1557.
22. Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Ann N Y Acad Sci 969: 323-339.
23. Russell FH (1898) An epidemic septicemic disease among frogs due to the Bacillus hydrophilus fuscus. J Am Med Assoc 30: 1442-1449.
24. Nyman S (1986) Mass mortality in larval Rana sylvatica attributable to the bacterium, Aeromonas hydrophila. J Herpetol 20: 196-201.
25. Mauel MJ, Miller DL, Frazier KS, Hines ME (2002) Bacterial pathogens isolated from cultured bullfrogs (Rana castebeiana). J Vet Diagn Invest 14: 431-433.
26. Frye FL (1985) An unusual epizootic of anuran aeromoniasis. J Am Vet Med Assoc 187: 1223-1224.
27. Bradford DF (1991) Mass mortality and extinction in a high-elevation population of Rana muscosa. J Herpetol 25: 174-177.
28. Carey C (2000) Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environ Health Perspect 108: 143-150.
29. Hird DH, Diesch SL, McKinnell RG, Gorham E, Martin FB, et al. (1981) Aeromonas hydrophila in wild-caught frogs and tadpoles (Rana pipiens) in Minnesota. Lab Anim Sci 31: 166-169.
30. Taylor SK, Green DE, Wright KMW, Whitaker BR (2001) Bacterial diseases. In: Wright KM, Whitaker BR, eds. Amphibian medicine and captive husbandry. Malbar, Florida: Krieger. pp 159-179.
31. Taylor SK, Williams ES, Mills KW (1999) Effects of malathion on disease susceptibility in Woodhouse's toads. J Wildl Dis 35: 536-541.
32. Travis J (1984) Anuran size at metamorphosis: experimental test of a model based on intraspecific competition. Ecology 65: 1155-1160.
33. Wilbur HM (1976) Density-dependent aspects or metamorphosis in Ambystoma and Rana sylvatica. Ecology 57: 1289-1296.
34. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis: nonnormal distributions of competitive ability reflect selection for facultative metamorphosis. Science 182: 1305-1314.
35. Wilbur HM (1982) Competition between tadpoles of Hyla femoralis and Hyla gratiosa in laboratory experiments. Ecology 63: 278-282.
36. Brockelman WY (1969) An analysis of density effects and predation in Bufo americanus tadpoles. Ecology 50: 632-644.
37. Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69: 184-192.
38. Smith DC (1987) Adult recruitment in chorus frogs: effects ofsize and date at metamorphosis. Ecology 68: 344-350.
39. Linder G, Krest SK, Sparling DW, eds (2003) Amphibian decline: An integrated analysis of multiple stressor effects. Pensacola, Florida: SETAC Press. 368 p.
40. Flajnik MF, Ohta Y, Greenberg AS, Salter-Cid I, Carrizosa A, et al. (1999) Two ancient allelic lineages at the single classical class I locus in the Xenopus MHC. J Immunol 163: 3826-3833.
41. Hazen TC, Fliermans CB, Hirsch RP, Esch GW (1978) Prevalence and distribution of Aeramonas hydrophila in the United States. Appl Environ Microbiol 36: 731-738.
42. Villinger J, Waldman B (2008) Self-referent MHC type matching in frog tadpoles. Proc R Soc Iond B 275: 1225-1230.
43. Grimholt U, Larsen S, Norchmo R, Midtlyng P, Kjoeglum, S, et al. (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55: 210-219.
44. Langefors, Å, Lohm J, Grahn M, Anderson Ø, von Schantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B 268: 479-485.
45. Lohm J, Grahn M, Langefors Å, Storset A, von Schantz T (2002) Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection. Proc R Soc Lond B 269: 2029-2033.
46. Miller KM, Winton JR, Schulze AD, Purcell MK, Ming TJ (2004) Major histocompatibility complex loci are associated with susceptibility of Atlantic salmon to infectious hematopoietic necrosis virus. Environ Biol Fishes 69: 307-316.
47. Pitcher TE, Neff BD (2006) MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol Ecol 15: 2357-2365.
48. Nauciel C, Ronco E, Guenet JL, Pla M (1988) Role of H-2 and non-H-2 genes in control ofbacterial clearance from the spleen in Salmonella typhimurium-infected mice. Infect Immun 56: 2407-2411.
49. Briles WE, Stone HA, Cole RK (1977) Marck's disease: effects of B histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195: 193-195.
50. Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, et al. (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B 272: 1511-1518.
51. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, et al. (1999) HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283: 1748-1752.
52. Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, et al. (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature 352: 595-600.
53. Tamouza R, Neonato M-G, Busson M, Marzais F, Girot R, et al. (2002) Infectious complications in sickle cell disease we influenced by HLA class II alleles. Hum Immunol 63: 194-199.
54. Apanius V, Penn D, Slev PR, Ruff LR, Potts W (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17: 179-224.
55. 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.
56. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
57. Gervasi SS, Foufopoulos J (2008) Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian. Funct Ecol 22: 100-108.
58. Lochmiller R, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87-98.
59. Salter-Cid L, Nonaka M, Flajnik MF (1998) Expression of MHC class Ia and class Ib during ontogeny: high expression in epithelia and coregulation of class Ia. and lmp7 genes. J Immunol 160: 2853-2861.
60. Du Pasquier L, Schwager J, Flajnik MF (1989) The immune system of Xenopus. Annu Rev Inummol 7: 251-275.
61. Villinger J (2007) Kin recognition and MHC discrimination in African clawed frog (Xenopus laevis) tadpoles. Ph.D. thesis, University of Canterbury, Christchurch, New Zealand.
62. Lewis K (1998) Pathogen resistance as the origin of kin altruism. J Theor Biol 193: 359-363.
63. Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunol Rev 166: 221-230.
64. Crump ML (1981) Variation in propagule size as a function of environmental uncertainty for three frogs. Am Nat 117: 724-737.
65. Crump ML (1984) Intraclutch egg size variability in Hyla crucifer (Anura: Hylidae). Copeia 1984: 302-308.
66. Dziminski MA, Alford RA (2005) Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs. Oecologia 146: 98-109.
67. Dziminski MA, Roberts JD (2006) Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana). J Evol Biol 19: 144-155.
68. Kaplan RH (1980) The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders ( Ambystoma). Evolution 34: 51-64.
69. Kaplan RH, Cooper WS (1984) The evolution of developmental plasticity in reproductive characteristics: an application of the "adaptive coin-flipping" principle. Am Nat 123: 393-410.
70. Todd B (2007) Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. Am Nat 170: 793-799.
71. Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318: 812-814
72. Retallick RWR, McCallum H, Speare R (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol 2(11): e351.
73. Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. J Wildl Manage 71: 435-444.
74. Rollins-Smith I, Doersam JK, Longcore JE, Taylor SK, Shamblin JC, et al. (2002) Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev Comp Immunol 26: 63-72.
75. Rollins-Smith L, Reinert LK, O'Leary CJ, Houston LE, Woodhams DC (2005) Antimicrobial peptide defenses in amphibian skin. Integr Comp Biol 45: 137-142.
76. Rollins-Smith LA (2001) Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol Res 23: 273-280.
77. Rollins-Smith L, Carey C, Longcore JE, Doersam JK, Boutte A, et al. (2002) Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev Comp Immunol 26: 471-479.
78. Rollins-Smith LA, Woodhams DC, Reinert LK, Vredenburg VT, Briggs CJ, et al. (2006) Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev Comp Immunol 30: 831-842.
79. Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422: 35.
80. Acevedo-Whitehouse K, Vincente J, Gortazar C, Höfle U, Fernández-de-Mera IG, et al. (2005) Genetic resistance to bovine tuberculosis in the Iberian wild boar. Mol Ecol 14: 3209-3217.
81. Pearman PB, Garner TWJ, Straub M, Greber UF (2004) Response of the Italian agile frog (Rana lalastei) to a Ranavirus, frog virus 3: a model for viral emergence in naïve populations. J Wildl Dis 40: 660-669.