Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents

Journal of Evolutionary Biology

Volumn 21, Issue 4, 2008, Pages 1144-1150

  Gouy De Bellocq J ^a,b   Charbonnel, N ^c   Morand, S ^d,e  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c CENTRE DE BIOLOGIE ET DE GESTION DES POPULATIONS   (France)

^d INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^e CIRAD   (France)

Author keywords

Comparative method; Helminths; Major histocompatibility complex diversity; Trans species polymorphism

Indexed keywords

CYTOCHROME B; HLA ANTIGEN CLASS 2; MICROSATELLITE DNA;

COEVOLUTION; COMPARATIVE STUDY; GENETIC DIFFERENTIATION; INTERSPECIFIC VARIATION; PARASITE; RODENT; SELECTION; SPECIES DIVERSITY; SPECIES RICHNESS;

ALLELE; ANIMAL; ARTICLE; GENETIC POLYMORPHISM; GENETICS; HAPLOTYPE; HELMINTH; IMMUNOLOGY; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; RODENT;

ALLELES; ANIMALS; CYTOCHROMES B; EVOLUTION, MOLECULAR; HAPLOTYPES; HELMINTHS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MICROSATELLITE REPEATS; PHYLOGENY; POLYMORPHISM, GENETIC; RODENTIA;

RODENTIA; VERMES;

EID: 45149108270     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01538.x     Document Type: Article

References (56)

1. Abu-Madi, M.A., Behnke, J.M., Lewis, J.W. Gilbert, F.S. 2000. Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. J. Helminthol. 74:7 15.
2. Altuvia, Y. Margalit, H. 2004. A structure-based approach for prediction of MHC-binding peptides. Methods 34:454 459.
3. Apanius, V., Penn, D., Slev, P.R., Ruff, L.R. Potts, W.K. 1997. The nature of selection on the major histocompatibility complex. Crit. Rev. Immunol. 17:179 224.
4. Babik, W., Durka, W. Radwan, J. 2005. Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol. Ecol. 14:4249 4257.
5. Berthier, K., Galan, M., Weber, A., Loiseau, A. Cosson, J.F. 2004. A multiplex panel of dinucleotide microsatellite markers for the water vole, Arvicola terrestris. Mol. Ecol. Notes 4:620 622.
6. Blake, J.A., Richardson, J.E., Bult, C.J., Kadin, J.A. Eppig, J.T. the members of the Mouse Genome Database Group. 2003. MGD: the mouse genome database. Nucleic Acids Res. 31:193 195.
7. Bryja, J., Galan, M., Charbonnel, N. Cosson, J.-F. 2006. Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in vole (Arvicolinae). Immunogenetics 58:191 202.
8. Chapman, C.A., Speirs, M.L., Gillespie, T.R., Holland, T. Austad, K.M. 2006. Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 68:397 409.
9. Chirhart, S.E., Honeycutt, R.L. Greenbaum, I.F. 2005. Microsatellite variation and evolution in the Peromyscus maniculatus species group. Mol. Phyl. Evol. 34:408 415.
10. Deffontaine, V., Libois, R., Kotlik, P., Sommer, R., Nieberding, C., Paradis, E., Searle, J.B. Michaux, J.R. 2005. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol. Ecol. 14:1727 1739.
11. Drózdz, J., Demiaszkiewicz, A.W. Lachowicz, J. 2004. Endoparasites of the beaver Castor fiber (L.) in northeast Poland. Helminthologia 41:99 101.
12. Durka, W., Babik, W., Ducroz, J.-F., Heidecke, D., Rosell, F., Samjaa, R., Saveljev, P., Stubbe, A., Ulevicius, A. Stubbe, M. 2005. Mitochondrial phylogeography of the Eurasian beaver Castor fiber L. Mol. Ecol. 14:3843 3856.
13. Feliu, C., Renaud, F., Catzeflis, F., Hugot, J.P., Durand, P. Morand, S. 1997. A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115:453 466.
14. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1 15.
15. Fink, S., Excoffier, L. Heckel, G. 2004. Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations. Mol. Ecol. 13:3501 3514.
16. Frandsen, J.C. Grundmann, A.W. 1961. Endoparasitism in isolated populations of rodents of the Lake Bonneville Basin, Utah. J. Parasitol. 47:391 396.
17. Froeschke, G. Sommer, S. 2005. MHC Class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol. Biol. Evol. 22:1254 1259.
18. Gandon, S. Michalakis, Y. 2000. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. R. Soc. Lond. B 267:985 990.
19. Garland, T.J., Harvey, P.H. Ives, A.R. 1992. Procedures for the analysis of comparative data using independents contrasts. Syst. Biol. 41:18 32.
20. Gauffre, B., Galan, M., Bretagnolle, V. Cosson, J.F. 2007. Polymorphic microsatellite loci and PCR multiplexing in the common vole, Microtus arvalis. Mol. Ecol. Notes 7:830 832.
21. Gerlach, G. Musolf, K. 2000. Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conserv. Biol. 14:1066 1074.
22. Gockel, J., Harr, B., Schlotterer, C., Arnold, W., Gerlach, G. Tautz, D. 1997. Isolation and characterization of microsatellite loci from Apodemus flavicollis (rodentia, muridae) and Clethrionomys glareolus (rodentia, cricetidae). Mol. Ecol. 6:597 599.
23. Gonzalez, M.T. Poulin, R. 2005. Spatial and temporal predictability of the parasite community structure of a benthic marine fish along its distributional range. Int. J. Parasitol. 35:1369 1377.
24. Harf, R. Sommer, S. 2005. Association between major histocompatibility complex class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. Mol. Ecol. 14:85 91.
25. Hurt, P., Walter, L., Sudbrak, R., Klages, S., Müller, I., Shiina, T., Inoko, H., Lehrach, H., Günther, E., Reinhardt, R. Himmelbauer, H. 2004. The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res. 14:631 639.
26. Jansa, S.A. Weksler, M. 2004. Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol. Phylogenet. Evol. 31:256 276.
27. Kelley, J., Walter, L. Trowsdale, J. 2005. Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683 695.
28. Klein, J. 1986. Natural History of the Major Histocompatibility Complex. Wiley, New York.
29. Klein, J. O'Huigin, C. 1994. MHC polymorphism and parasites. Philos. Trans. R. Soc. B 346:351 357.
30. Klein, J., Sato, A., Nagl, S. O'hUigin, C. 1998. Molecular trans-species polymorphism. Annu. Rev. Ecol. Syst. 29:1 21.
31. Martin, J.L. Huffman, D.G. 1980. An analysis of the community and population dynamics of the helminths of Sigmodon hispidus (Rodentia: Criceditae) from three Central Texas vegetational regions. Proc. Helminthol. Soc. Wash. 47:247 255.
32. Meyer, D. Thomson, G. 2001. How selection shapes variation of the human major histocompatibility complex: a review. Ann. Hum. Genet. 65:1 26.
33. Meyer-Lucht, Y. Sommer, S. 2005. MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol. Ecol. 14:2233 2243.
34. Michaux, J., Magnanou, E., Paradis, E., Nieberding, C. Libois, R. 2003. Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Paleartic region. Mol. Ecol. 12:685 697.
35. Michaux, J.R., Filippucci, M.-G. Libois, R. 2004. Phylogeographic history of the Yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Mol. Phylogenet. Evol. 32:188 198.
36. Miller, K.M., Ming, T.J., Schulze, A.D. Withler, R.E. 1999. Denaturing gradient gel electrophoresis (DGGE): a rapid and sensitive technique to screen nucleotide sequence variation in populations. BioTechniques 27:1016 1030.
37. Miller, K.M., Kaukinen, K.H., Beacham, T.D. Withler, R.E. 2001. Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111:237 257.
38. Morand, S. Poulin, R. 1998. Density, body mass and parasite species richness of terrestrial mammals. Evol. Ecol. 12:717 727.
39. Musolf, K., Meyer-Lucht, Y. Sommer, S. 2004. Evolution of MHC-DRB class II polymorphism in the genus Apodemus and a comparison of DRB sequences within the family Muridae (Mammalia: Rodentia). Immunogenetics 56:420 426.
40. Nieberding, C., Libois, R., Douady, C.J., Morand, S. Michaux, J.R. 2005. Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages? Mol. Ecol. 14:765 779.
41. Oliver, M.K. Piertney, S.B. 2006. Isolation and characterization of a MHC class II DRB locus in the European water vole (Arvicola terrestris). Immunogenetics 58:390 395.
42. Pfau, R.S., van den Bussche, R.A. McBee, K. 2001. Population genetics of the hispid cotton rat (Sigmodon hispidus): patterns of genetic diversity at the major histocompatibility complex. Mol. Ecol. 10:1939 1945.
43. Poulin, R. 2004. Parasites and the neutral theory of biodiversity. Ecography 27:119 123.
44. Prugnolle, F., Manica, A., Charpentier, M., Guégan, J.-F., Guernier, V. Balloux, F. 2006. Pathogen-driven selection and worldwide HLA class I diversity. Curr. Biol. 15:1022 1027.
45. Purvis, A. Rambaut, A. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput. Appl. Biosci. 11:247 251.
46. Rambau, R.V., Robinson, T.J. Stanyon, R. 2003. Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Mol. Phylogenet. Evol. 28:564 575.
47. Richman, A.D., Herrera, L.G. Nash, D. 2001. MHC class II beta sequence diversity in the deer mouse (Peromyscus maniculatus): implications for models of balancing selection. Mol. Ecol. 10:2765 2773.
48. Sanchez-Mazas, A., Djoulah, S., Busson, M., Le Monnier de Gouville, I., Poirier, J.C., Dehay, C., Charron, D., Excoffier, L., Schneider, S., Langaney, A., Dausset, J. Hors, J. 2000. A linkage disequilibrium map of the MHC region based on the analysis of 14 loci haplotypes in 50 French families. Eur. J. Hum. Genet. 8:33 41.
49. Sorci, G., Skarstein, F., Morand, S. Hugot, J.-P. 2004. Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites. Proc. R. Soc. Lond. B 270:2481 2484.
50. Steppan, S.J., Adkins, R.M., Spinks, P.Q. Hale, C. 2005. Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol. Phylogenet. Evol. 37:370 388.
51. Sunnucks, P., Wilson, A.C.C., Beheregaray, L.B., Zenger, K., French, J. Taylor, A.C. 2000. SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol. Ecol. 9:1699 1710.
52. Tellier, A. Brown, J.K.M. 2007. Stability of genetic polymorphism in host-parasite interactions. Proc. R. Soc. Lond. B 274:809 817.
53. Wakelin, D. 1988. Genetic control of immunity to helminth infections. In:Parasitology in Focus (H. Mehlhorn, ed. pp. 651 670. Springer, Berlin.
54. Wegner, K.M., Reusch, T.B.H. Kalbe, M. 2003. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J. Evol. Biol. 16:224 232.
55. Westerdahl, H., Hansson, B., Bensch, S. Hasselquist, D. 2004. Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J. Evol. Biol. 17:485 492.
56. Zheng, X., Arbogast, B.S. Kenagy, G.J. 2003. Historical demography and genetic structure of sister species: deermice (Peromyscus) in the North American temperate rain forest. Mol. Ecol. 12:711 724.