Quantitative disease resistance: To better understand parasite-mediated selection on major histocompatibility complex

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1728, 2012, Pages 577-584

  Westerdahl, Helena ^a   Asghar, Muhammad ^a   Hasselquist, Dennis ^a   Bensch, Staffan ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Avian malaria; Major histocompatibility complex (MHC) class I; Qualitative resistance; Quantitative resistance; Susceptibility allele

Indexed keywords

ALLELE; AVIFAUNA; DATA SET; DISEASE PREVALENCE; DISEASE RESISTANCE; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; INFECTIOUS DISEASE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALARIA; NATURAL SELECTION; QUANTITATIVE ANALYSIS; SONGBIRD;

EID: 84055222357     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0917     Document Type: Article

References (58)

1. De Roode, J. C., Gold, L. R. & Altizer, S. 2007 Virulence determinants in a natural butterfly-parasite system. Parasitology 134, 657-668. (doi:10.1017/S0031182006002009)
2. Greenwood, B. M., Marsh, K. & Snow, R. 1991 Why do some African children develop severe malaria? Parasitol. Today 7, 277-281. (doi:10.1016/0169-4758(91)90096-7)
3. Miller, L. H., Baruch, D. I., Marsh, K. & Doumbo, O. K. 2002 The pathogenic basis of malaria. Nature 415, 673-679. (doi:10.1038/415673a)
4. Bensch, S. & Akesson, S. 2003 Temporal and spatial variation of haemoprotozoans in Scandinavian willow warblers. J. Parasitol. 89, 388-391. (doi:10.1645/00223395(2003)089[0388:TASVOH]2.0.CO;2)
5. Yohannes, E., Hansson, B., Lee, R. W., Waldenström, J., Westerdahl, H., Akesson, M., Hasselquist, D. & Bensch, S. 2008 Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia 158, 299-306.(doi:10.1007/s00442-008-1138-3)
6. Beldomenico, P. M. & Begon, M. 2010 Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol. Evol. 25, 21-27.(doi:10.1016/j.tree.2009.06.015)
7. Bergelson, J. & Purrington, C. B. 1996 Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536-558.(doi:10.1086/285938)
8. Gandon, S. & Michalakis, Y. 2000 Evolution of parasite virulence against qualitative or quantitative form of resistance. Proc. R. Soc. Lond. B 267, 985-990.(doi:10.1098/rspb.2000.1100)
9. 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.(doi:10.1046/j.1420-9101.2003.00531.x)
10. Piertney, S. B. & Oliver, M. K. 2006 The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7-21.(doi:10.1038/sj.hdy.6800724)
11. Sommer, S. 2005 The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front. Zool. 2, 1-18.(doi:10.1186/1742-9994-2-1)
12. Purrington, C. B. & Bergelson, J. 1999 Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana. Am. Nat. 154, 82-91.(doi:10.1086/303285)
13. Westerdahl, H. 2007 Passerine MHC: genetic variation and disease resistance in the wild. J. Ornithol. 148, 469-477.(doi:10.1007/s10336-007-0230-5)
14. Kosmrlj, A. et al. 2010 Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465, 350-354.(doi:10.1038/nature08997)
15. Hill, A. V. S. et al. 1991 CommonWest African HlA antigens are associated with protection from severe malaria. Nature 352, 595-600.(doi:10.1038/352595a0)
16. Klein, J. 1986 Natural history of the major histocompatibility complex, 1st edn. New York, NY: John Wiley and Sons.
17. Hedrick, P.W. 2002 Pathogen resistance and genetic variation at MHC loci. Evolution 56, 1902-1908.(doi:10.1111/j.0014-3820.tb00116.x)
18. Worley, K., Collet, J., Spurgin, L. G., Cornwallis, C., Pizzari, T. & Richardson, D. S. 2010 MHC heterozygosity and survival in red junglefowl. Mol. Ecol. 19, 3064-3075.(doi:10.1111/j.1365-294X.2010.04724.x)
19. Fujisawa, T. et al. 2006 MHC-linked susceptibility to type 1 diabetes in the NOD mouse: further localization of Idd16 by subcongenic analysis. Ann. NY Acad. Sci. 1079, 118-121.(doi:10.1196/annals.1375.017)
20. Zenewicz, L. A., Abraham, C., Flavell, R. A. & Cho, J. H. 2010 Unraveling the genetics of autoimmunity. Cell 140, 791-797.(doi:10.1016/j.cell.2010.03.003)
21. Bonneaud, C., Perez-Tris, J., Federici, P., Chastel, O. & Sorci, G. 2006 Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60, 383-389.(doi:10.1111/j.0014-3820.2006.tb01114.x)
22. Loiseau, C., Zoorob, R., Garnier, S., Birard, J., Federici, P., Julliard, R. & Sorci, G. 2008 Antagonistic effects of a MHC class I allele on malaria-infected house sparrows. Ecol. Lett. 11, 258-265.(doi:10.1111/j.1461-0248.2007.01141.x)
23. Loiseau, C., Zoorob, R., Robert, A., Chastel, O., Julliard, R. & Sorci, G. 2011 Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus). Proc. R. Soc. B 278, 1264-1272.(doi:10.1098/rspb.2010.1968)
24. Westerdahl, H., Waldenstrom, J., Hansson, B., Hasselquist, D., von Schantz, T. & Bensch, S. 2005 Associations between malaria and MHC genes in a migratory songbird. Proc. R. Soc. B 272, 1511-1518.(doi:10.1098/rspb.2005.3113)
25. Valkiunas, G. 2005 Avian malaria parasites and other haemosporidia. Boca Raton, FL: CRC Press.
26. Hellgren, O., Krizanauskiene, A., Valkiunas, G. & Bensch, S. 2007 Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J. Parasitol. 93, 889-896.(doi:10.1645/GE-1051R1.1)
27. Waldenstrom, J., Bensch, S., Kiboi, S., Hasselquist, D. & Ottosson, U. 2002 Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol. Ecol. 11, 1545-1554.(doi:10.1046/j.1365-294X.2002.01523.x)
28. Palinauskas, V., Valkiunas, G., Bolshakov, C. V. & Bensch, S. 2008 Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp. Parasitol. 120, 372-380.(doi:10.1016/j.exppara.2008.09.001)
29. Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiunas, G. & Bensch, S. 2008 Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Exp. Parasitol. 119, 99-110.(doi:10.1016/j.exppara.2007.12.018)
30. Mackinnon, M. J. & Read, A. F. 2003 The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology 126, 103-112.(doi:10.1017/S003118200200272X)
31. Atkinson, C. T. & van Riper, C. 1991 Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In Bird-parasite interactions (eds J. E. Loye & M. Zuk), pp. 19-48. New York, NY: Oxford University Press.
32. Bensch, S., Waldenstrom, J., Jonzen, N., Westerdahl, H., Hansson, B., Sejberg, D. & Hasselquist, D. 2007 Temporal dynamics and diversity of avian malaria parasites in a single host species. J. Anim. Ecol. 76, 112-122.(doi:10.1111/j.1365-2656.2006.01176.x)
33. Westerdahl, H., Hansson, B., Bensch, S. & Hasselquist, D. 2004a Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J. Evol. Biol. 17, 485-492.(doi:10.1111/j.1420-9101.2004.00711.x)
34. Westerdahl, H., Wittzell, H. & von Schantz, T. 1999 Polymorphism and transcription of MHC class I genes in a passerine bird, the great reed warbler. Immunogenetics 49, 158-170.(doi:10.1007/s002510050477)
35. Westerdahl, H., Wittzell, H., von Schantz, T. & Bensch, S. 2004 MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. Heredity 92, 534-542.(doi:10.1038/sj.hdy.6800450)
36. Bensch, S. & Hasselquist, D. 1991 Territory infidelity in the polygynous great reed warbler Acrocephalus arundinaceus: the effect of variation in territory attractiveness. Anim. Ecol. 60, 857-871.(doi:10.2307/5418)
37. Bensch, S., Hasselquist, D. & von Schantz, T. 1994 Genetic similarity between parents predicts hatching failure: non-incestuous inbreeding in the great reed warbler? Evolution 48, 317-326.(doi:10.2307/2410095)
38. Sambrook, J., Fritsch, E. F. & Maniatis, T. 1989 Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
39. Asghar, M., Hasselquist, D. & Bensch, S. 2011 Are chronic haemosporidian infections costly in wild birds? J. Avian Biol. 42.(doi:10.1111/j.1600-0587.2011.05281.x)
40. Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S. & Haussler, D. 2004 Ultraconserved elements in the human genome. Science 304, 1321-1325.(doi:10.1126/science.1098119)
41. Myers, R. M., Maniatis, T. & Lerman, L. S. 1987 Detection and localization of single base changes by denaturing gradient gel-electrophoresis. Methods Enzymol. 155, 501-527.(doi:10.1016/0076-6879(87)55033-9)
42. Nowak, M. A., Tarczyhornoch, K. & Austyn, J. M. 1992 The optimal number of major histocompatibility complex- molecules in an individual. Proc. Natl Acad. Sci. USA 89, 10896-10899. (doi:10.1073/pnas.89.22.10896)
43. Langefors, A., Lohm, J., Grahn, M., Andersen, O. & 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.(doi:10.1098/rspb.2000.1378)
44. Madsen, T. & Ujvari, B. 2006 MHC class I variation associates with parasite resistance and longevity in tropical pythons. J. Evol. Biol. 19, 1973-1978.(doi:10.1111/j.1420-9101.2006.01158.x)
45. Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. & Milinski, M. 2003 Parasite selection for immunogenetic optimality. Science 301, 1343.(doi:10.1126/science.1088293)
46. 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.(doi:10.1093/molbev/msi112)
47. Kloch, A., Babik, W., Bajer, A., Sinski, E. & Radwan, J. 2010 Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Mol. Ecol. 19, 255-265.(doi:10.1111/ j.1365-294X.2009.04476.x)
48. 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.(doi:10.1111/j.1365-294X.2005.02557.x)
49. Meyer-Lucht, Y. & Sommer, S. 2009 Number of MHC alleles is related to parasite loads in natural populations of yellow necked mice, Apodemus flavicollis. Evol. Ecol. Res. 11, 1085-1097.
50. Rook, G. A. W. 2009 Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126, 3-11.(doi:10.1111/j.1365-2567.2008.03007.x)
51. Todesco, M. et al. 2010 Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465, 632-636.(doi:10.1038/nature09083)
52. Spurgin, L. G. & Richardson, D. S. 2010 How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. R. Soc. B 277, 979-988.(doi:10.1098/rspb.2009.2084)
53. Nowak, M. A., Tarczyhornoch, K. & Austyn, J. M. 1992 The optimal number of major histocompatibility complex- molecules in an individual. Proc. Natl Acad. Sci. USA 89, 10896-10899.
54. Woelfing, B., Traulsen, A., Milinski, M. & Boehm, T. 2009 Does intra-individual major histocompatibility complex diversity keep a golden mean? Phil. Trans. R. Soc. B 364, 117-128.(doi:10.1098/rstb.2008.0174)
55. Roder, G., Geironson, L., Darabi, A., Harndahl, M., Schafer-Nielsen, C., Skjodt, K., Buus, S. & Paulsson, K. 2009 The outermost N-terminal region of tapasin facilitates folding of major histocompatibility complex class I. Eur. J. Immunol. 39, 2682-2694.(doi:10.1002/eji.200939364)
56. 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.(doi:10.1111/j.1365-294X.2004.02402.x)
57. Madsen, T. & Ujvari, B. 2006 MHC class I variation associates with parasite resistance and longevity in tropical pythons. J. Evol. Biol. 19, 1973-1978.(doi:10.1111/j.1420-9101.2006.01158.x)
58. Moller, A. P. & Nielsen, J. T. 2007 Malaria and risk of predation: a comparative study of birds. Ecology 88, 871-881.(doi:10.1890/06-0747)