Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus

Evolution

Volumn 59, Issue 2, 2005, Pages 439-450

  Schad, J ^a   Ganzhorn, J U ^a   Sommer, S ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Lemur; Madagascar; Major histocompatibility complex; Microcebus murinus; Parasite load

Indexed keywords

HOST-PARASITE INTERACTION; MAJOR HISTOCOMPATIBILITY COMPLEX; PARASITE INTENSITY; PRIMATE;

INDIAN OCEAN; INDIAN OCEAN ISLANDS; MADAGASCAR; OCEANIC REGIONS; WORLD;

ANIMALIA; LEMUR; LEMURIDAE; MICROCEBUS MURINUS; PRIMATES; STREPSIRHINI;

EID: 14844365794     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2005.tb01002.x     Document Type: Article

References (72)

1. Arkush, K. D., A. R. Giese, H. L. Mendonca, A. M. McBride, G. D. Marty, and P. W. Hedrick. 2002. Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tsawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can. J. Fish. Aquat. Sci. 59:966-975.
2. Behnke, J. M., and F. N. Wahid. 1991. Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 linked genes determine worm survival. Parasitology 103:157-164.
3. Bergstrom, T., and U. Gyllensten. 1995. Evolution of MHC class II polymorphism: The rise and fall of class II gene function in primates. Immunol. Rev. 143:13-31.
4. Bernatchez, L., and C. Landry. 2003. MHC studies in nonmodel vertebrates: What have we learned about natural selection in 15 years? J. Evol. Biol. 16:363-377.
5. Borghans, J. A. M., J. B. Beltman, and R. J. de Boer. 2004. MHC polymorphism under host-pathogen coevolution. Immunogenetics 55:732-739.
6. Brown, J. H., T. S. Jardetzky, M. A. Saper, B. Samraoui, P. J. Bjorkman, and D. C. Wiley. 1988. A hypothetical model of foreign antigen binding site of class II histocompatibility molecules. Nature 332:845-850.
7. Brown, J. H., T. S. Jardetzky, J. C. Gorga, L. J. Stern, R. G. Urban, J. L. Strominger, and D. C. Wiley. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33-39.
8. Buitkamp, J., P. Filmether, M. J. Stear, and J. T. Epplen. 1996. Class I and class II major histocompatibility complex alleles are associated with faecal egg counts following natural, predominantly Ostertagia circumcincta, infection. Parasitol. Res. 82:693-696.
9. Carrington, M., G. W. Nelson, M. P. Martin, T. Kissner, D. Vlahov, J. J. Goedert, R. Kaslow, S. Buchbinder, K. Hoots, and S. J. O'Brien. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283:1748-1752.
10. Cassinello, J., M. Gomendio, and E. R. S. Roldan. 2001. Relationship between coefficient of inbreeding and parasite burden in endangered gazelles. Conserv. Biol. 15:1171-1174.
11. Chen, C. Y., S. A. Cohen, M. B. Zaleski, and B. Albini. 1992. Genetic control of streptococcus-induced hepatic granulomatous lesions in mice. Immunogenetics 36:28-32.
12. Coltman, D. W., J. G. Pilkington, J. A. Smith, and J. M. Pemberton. 1999. Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259-1267.
13. De Boer, R. J., J. A. M. Borghans, M. Van Boven, C. Kesmir, and F. J. Weissing. 2004. Heterozygote advantage fails to explain the high degree of polymorphism of the MHC. Immunogenetics 55:725-731.
14. Dobson, A. P., P. J. Hudson, and A. M. Lyles. 1992. Macroparasites: It's a wormy world. Pp. 329-248 in M. J. Crawley, ed. Natural enemies. Blackwell Scientific, Oxford, U.K.
15. Doherty, P. C., and R. M. Zinkernagel. 1975. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50-52.
16. Edwards, S. V., and W. K. Potts. 1996. Polymorphism of genes in the major histocompatibility complex (MHC): Implications for conservation genetics of vertebrates. Pp. 214-237 in T. B. Smith and R. K. Wayne, eds. Molecular genetic approaches in conservation. Oxford Univ. Press, New York.
17. Frank, S. A. 2002. Immunology and the evolution of infectious disease. Princeton Univ. Press, Princeton, NJ.
18. Ganzhorn, J. U., and J. Schmid. 1998. Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int. J. Primatol. 19:785-796.
19. Ganzhorn, J. U., P. P. Lowry II, G. E. Schatz, and S. Sommer. 2001. The biodiversity of Madagascar: one of the world's hottest hotspots on its way out. Orynx 35:1-3.
20. Godot, V., S. Harraga, I. Beurton, P. Tiberghien, E. Sarciron, B. Gottstein, and D. A. Vuitton. 2000. Resistance/susceptibility to Echinococcus multilocularis infection and cytocine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clin. Exp. Immunol. 121:491-498.
21. Gulland, F. M. D. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105:493-503.
22. Gulland, F. M. D., S. D. Albon, J. M. Pemberton, P. R. Moorcroft, and T. H. Clutton-Brock. 1993. Parasite associated polymorphism in a cyclic ungulate population. Proc. R. Soc. Lond. B 254:7-13.
23. Harf, R., and S. Sommer. 2005. Association between MHC Class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. Mol. Ecol. 14:85-91.
24. Hedrick, P. W. 1994. Evolutionary genetics at the major histocompatibility complex. Am. Nat. 143:945-964.
25. Hedrick, P. W., T. J. Kim, and K. M. Parker. 2001. Parasite resistance and genetic variation in the endangered Gi1a topminnow. Anim. Conserv. 4:103-109.
26. Hill, A. V. S. 1999. Defence by diversity. Nature 398:668-669.
27. Hill, A. V. S., C. E. M. Allsopp, and D. Kwiatkowski. 1991. Common West African HLA antigens associated with protection from severe malaria. Nature 352:595-600.
28. Hughes, A. L., and M. Nei. 1988. Pattern of nucleotide substitution at major histocompatibility complex class-I loci reveals overdominant selection. Nature 335:167-170.
29. _. 1989. Nucleotide substitution at major histocompatibility complex class II loci: Evidence for overdominant selection. Proc. Natl. Acad. Sci. USA 86:948-962.
30. Hughes, A. L., and M. Yeager. 1998. Natural selection at major histocompatibility complex loci of vertebrates. Annu. Rev. Genet. 32:415-434.
31. Jeffery, K. J., and C. R. Bangham. 2000. Do infectious diseases drive MHC diversity? Microbes Infect. 2:1335-1341.
32. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-132 in H. N. Munro, ed. Mammalian protein metabolism. Academic Press, New York.
33. Klein, J. 1986. Natural history of the major histocompatibility complex. Wiley and Sons, New York.
34. Kumar, S., K. Tamura, I. B. Jakobson, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Arizona State University, Tempe, AZ.
35. Langefors, A., J. Lohm, M. Grahn, O. Andersen, and T. Von Schantz. 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.
36. Lohm, J., M. Grahn, A. Langefors, O. Andersen, A. Storset, and T. von Schantz. 2002. Experimental evidence for major histocompatibility complex allele-specific resistance to a bacterial infection. Proc. R. Soc. Lond. B 269:2029-2033.
37. Maizels, R. M., and M. Yazdanbakhsh. 2003. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat. Rev. 3:733-744.
38. May, R. M., and R. M. Anderson. 1990. Parasite-host coevolution. Parasitology 100:89-101.
39. Meyer-Lucht, Y. 2003. Einfluss von Verstädterung auf Populationsstruktur, genetische Variabilität und Parasitenbefall bei der Gelbhalsmaus (Apodemus flavicollis). Master's thesis, Universität Hamburg, Germany.
40. Nei, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
41. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the number of synonymous and non-synonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
42. Nunn, C. L., S. Altizer, K. E. Jones, and W. Sechrest. 2003. Comparative tests of parasite species richness in primates. Am. Nat. 162:597-614.
43. Orita, M., H. Iwahana, H. Kanazawa, K. Hayashi, and T. Sekiya. 1989. Detection of polymorphism of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc. Natl. Acad. Sci. USA 86:2766-2770.
44. Paterson, S., K. Wilson, and J. M. Pemberton. 1998. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Evolution. 95:3714-3719.
45. Penn, D. J. 2002. The scent of genetic compatibility: Sexual selection and the major histocompatibility complex. Ethology 108:1-21.
46. Penn, D. J., K. Damjanovich, and W. K. Potts. 2002. MHC heterozygosity confers a selective advantage against multi-strain infections. Proc. Natl. Acad. Sci. 99:11260-11264.
47. Penn, D. J., and W. K. Potts. 1999. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153:145-164.
48. Potts, W. K., and E. K. Wakeland. 1993. Evolution of MHC genetic diversity: A tale of incest, pestilence and sexual preference. Trends. Genet. 9:408-412.
49. Poulin, R., D. Mouillot, and M. George-Nascimento. 2003. The relationship between species richness and productivity in metazoen parasite communities. Oecologia 137:277-285.
50. Quinnell, R. J. 2003. Genetics of susceptibility to human helminth infection. Int. J. Parasitol. 33:1219-1231.
51. Ramanamanjato, J.-B., and J. U. Ganzhorn. 2001. Effects of forest fragmentation, introduced Rattus rattus and the role of exotic tree plantations and secondary vegetation for the conservation of an endemic rodent and a small lemur in littoral forests of southeastern Madagascar. Anim. Conserv. 4:175-183.
52. Raymond, M., and F. Roussel. 1995. An exact test for population differentiation. Evolution 49:1280-1283.
53. Reusch, T. B. H., M. A. Häberli, P. B. Aeschliemann, and M. Milinski. 2001. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300-302.
54. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
55. Rüdel, N. 2004. Auswirkungen von Degradation und Fragmentation madagassischer Küstenregenwälder auf graue Mausmakis (Microcebus murinus). Master's thesis. University of Hamburg, Germany.
56. Sachs, I. 1992. Angewandte statistik. Springer Verlag, Berlin.
57. Schad, J., S. Sommer, and J. U. Ganzhorn. 2004. MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conserv. Genet. 5:299-309.
58. Sher, A., S. Hieny, and S. James. 1984. Mechanisms of protective immunity against S. mansoni infection in mice vaccinated with irradiated cercariae: VI. Influence of the major histocompatibility complex. Parasitol. Immunol. 6:319-328.
59. Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequin. A software for population genetics data analysis. Ver. 2.000. Geneva.
60. Sloss, M. W., R. L. Kemp, and A. Zajak. 1994. Veterinary clinical parasitology. Iowa State Univ. Press, Ames, IA.
61. Sommer, S. 2003. Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol. Ecol. 12:2845-2851.
62. Sommer, S., and H. Tichy. 1999. Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antinema, the endangered, largest endemic Malagasy rodent. Mol. Ecol. 8:1259-1272.
63. Sommer, S., D. Schwab, and J. U. Ganzhorn. 2002. MHC diversity of endemic Malagasy rodents in relation to range contraction and social system. Behav. Ecol. Sociobiol. 51:214-221.
64. Stear, M. J., K. Bairden, J. L. Duncan, P. H. Holmes, Q. A. Mckellar, M. Park, S. Strain, M. Murray, S. C. Bishop, and G. Gettinby. 1997. How hosts control worms. Nature 389:27.
65. Stear, M. J., M. Park, and S. C. Bishop. 1996. The key components of resistance to Ostertagia circumcincta in lambs. Parasitol. Today 12:438-441.
66. Summers, K., S. McKeon, J. Sellars, M. Keusenkothen, J. Morris, D. Gloeckner, C. Pressley, B. Price, and H. Snow. 2003. Parasitic exploitation as an engine of diversity. Biol. Rev. 78:639-675.
67. Takahata, N., and M. Nei. 1990. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967-978.
68. Thursz, M. R., D. Kwiatkowski, C. E. M. Allsopp, B. M. Greenwood, H. C. Thomas, and A. V. S. Hill. 1995. Association between an MHC class II allele and clearance of hepatitis B virus in Gambia. N. Engl. J. Med. 332:1065-1069.
69. Thursz, M. R., H. C. Thomas, B. M. Greenwood, and A. V. Hill. 1997. Heterozygote advantage for HLA class II-type in hepatitis virus infection. Nat. Genet. 17:11-12.
70. Von Schantz, T., H. Wittzell, G. Goransson, M. Grahn, and K. Persson. 1996. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc. R. Soc. Lond. B 263:265-271.
71. Wegner, K. M., T. B. H. Reusch, and M. Kalbe. 2003. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J. Evol. Biol. 16:224-232.
72. Wright, S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395-420.