Balancing selection, sexual selection and geographic structure in MHC genes of Great Snipe

Genetica

Volumn 138, Issue 4, 2010, Pages 453-461

  Ekblom, Robert ^a,b   Sæther, Stein Are ^c   Fiske, Peder ^d   Kålås, John Atle ^d   Höglund, Jacob ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF OSLO   (Norway)

^d NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

Author keywords

Balancing selection; Bird; Major histocompatibility complex; Mate choice; Rare allele advantage

Indexed keywords

ALLELE; ANIMAL; ARTICLE; CHARADRIIFORMES; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; GEOGRAPHY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATE CHOICE; POPULATION GENETICS;

ALLELES; ANIMALS; CHARADRIIFORMES; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; GEOGRAPHY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATING PREFERENCE, ANIMAL; POLYMORPHISM, GENETIC; SELECTION, GENETIC;

AVES; GALLINAGO MEDIA;

EID: 77949289835     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-008-9335-x     Document Type: Article

References (77)

1. Arcaro KF, Eklund A (1999) A review of MHC-based mate preferences and fostering experiments in two congenic strains of mice. Genetica 104: 241-244. doi: 10. 1023/A: 1026465421201.
2. Bacon LD (1987) Influence of the major histocompatibility complex on disease resistance and productivity. Poult Sci 66: 802-811.
3. Bodmer W (1972) The evolutionary significance of the HLA-system. Nature 237: 139-145. doi: 10. 1038/237139a0.
4. Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorcil G (2006a) Complex MHC-based mate choice in a wild passerine. Proc R Soc B Biol Sci 273: 1111-1116. doi: 10. 1098/rspb. 2005. 3325.
5. Bonneaud C, Perez-Tris J, Federici P, Chastel O, Sorci G (2006b) MHC alleles confer local resistance to malaria in a wild passerine. Evol Int J Org Evol 60: 383-389.
6. Brown ME (1996) Assessing body condition in birds. Curr Ornithol 13: 67-135.
7. Brown JL (1999) The new heterozygosity theory of mate choice and the MHC. Genetica 104: 215-221. doi: 10. 1023/A: 1026409220292.
8. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33-39. doi: 10. 1038/364033a0.
9. Brya J, Charbonnel N, Berthier K, Galan M, Cosson J-F (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16: 5084-5097. doi: 10. 1111/j. 1365-294X. 2007. 03584. x.
10. Charbonnel N, Pemberton J (2005) A long-term genetic survey of an ungulate population reveals balancing selection acting on MHC through spatial and temporal fluctuations in selection. Heredity 95: 377-388. doi: 10. 1038/sj. hdy. 6800735.
11. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res Camb 70: 155-174.
12. Clarke B, Kirby DRS (1966) Maintenance of histocompatibility polymorphisms. Nature 211: 999-1000. doi: 10. 1038/211999a0.
13. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256: 50-52. doi: 10. 1038/256050a0.
14. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13: 305-311. doi: 10. 1016/S0169-5347(98)01416-5.
15. Ekblom R, Grahn M, Höglund J (2003) Patterns of polymorphism in the MHC class II of a non-passerine bird, the great snipe (Gallinago media). Immunogenetics 54: 734-741.
16. Ekblom R, Sæther SA, Grahn M, Fiske P, Kålås JA, Höglund J (2004) Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Mol Ecol 13: 3821-3828. doi: 10. 1111/j. 1365-294X. 2004. 02361. x.
17. Ekblom R, Sæther SA, Jacobsson P, Fiske P, Sahlman T, Grahn M, Kålås JA, Höglund J (2007) Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 16: 1439-1451. doi: 10. 1111/j. 1365-294X. 2007. 03281. x.
18. Fiske P, Kålås JA (1995) Mate sampling and copulation behaviour of great snipe females. Anim Behav 49: 209-219. doi: 10. 1016/0003-3472(95)80169-3.
19. Fiske P, Kålås JA, Sæther SA (1994) Correlates of male mating success in the lekking great snipe. Behav Ecol 5: 210-218. doi: 10. 1093/beheco/5. 2. 210.
20. Forsberg LA, Dannewitz J, Petersson E, Grahn M (2007) Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout-females fishing for optimal MHC dissimilarity. J Evol Biol 20: 1859-1869. doi: 10. 1111/j. 1420-9101. 2007. 01380. x.
21. Garrigan D, Hedrick PW (2003) Detecting adaptive molecular polymorphism: lessons from the mhc. Evol Int J Org Evol 57: 1707-1722.
22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41: 95-98.
23. Hauswaldt JS, Stuckas H, Pfautsch S, Tidemann R (2007) Molecular characterization of MHC class II in a nonmodel anuran species, the fire-bellied toad Bombina bombina. Immunogenetics 59: 479-491. doi: 10. 1007/s00251-007-0210-1.
24. Hedrick PW (1999) Balancing selection and MHC. Genetica 104: 207-214. doi: 10. 1023/A: 1026494212540.
25. Hedrick PW, Black FL (1997) HLA and mate selection: no evidence in south amerindians. Am J Hum Genet 61: 505-511. doi: 10. 1086/515519.
26. Hedrick PW, Kim TJ (2000) Genetics of complex polymorphisms: parasites and maintenance of the major histocompatibility complex variation. In: Singh RS, Krimbas CB (eds) Evolutionary genetics. from molecules to morphology. Cambridge University Press, Cambridge, pp 204-234.
27. Hedrick PW, Loeschcke V (1996) MHC and mate selection in humans? Trends Ecol Evol 11: 24. doi: 10. 1016/0169-5347(96)80237-0.
28. Hill AVS (1991) HLA associations with malaria in africa: some implications for MHC evolution. In: Klein J, Klein D (eds) Molecular evolution of the major histocompatibility complex. Springer, Berlin Heidelberg, pp 403-419.
29. Höglund J, Kålås JA, Løfaldli L (1990) Sexual polymorphism in the lekking Great Snipe. Ornis Scand 21: 1-6. doi: 10. 2307/3676372.
30. Hughes AL, Hughes MK (1995) Natural selection on the peptide-binding regions of major histocompatibility complex. Immunogenetics 42: 233-243. doi: 10. 1007/BF00176440.
31. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: Evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958-962. doi: 10. 1073/pnas. 86. 3. 958.
32. Hughes AL, Nei M (1992) Models of host-parasite interaction and MHC polymorphism. Genetics 132: 863-864.
33. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32: 415-435. doi: 10. 1146/annurev. genet. 32. 1. 415.
34. Jin K, Speed TP, Thomson G (1995) Tests of random mating for a highly polymorphic locus: application to HLA data. Biometrics 51: 1064-1076. doi: 10. 2307/2533005.
35. Jordan WC, Bruford MW (1998) New perspectives on mate choice and the MHC. Heredity 81: 127-133. doi: 10. 1038/sj. hdy. 6884281.
36. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular evolutionary genetics analysis software. Arizona State University, Tempe.
37. Lamont SJ (1991) Immunogenetics and the major histocompatibility complex. Vet Immunol Immunopathol 30: 121-127. doi: 10. 1016/0165-2427(91)90013-3.
38. Langefors Å, Lohm J, Grahn M, Andersen O, von Shantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B Biol Sci 268: 479-485. doi: 10. 1098/rspb. 2000. 1378.
39. Meyer D, Thomson G (2001) How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 65: 1-26. doi: 10. 1046/j. 1469-1809. 2001. 6510001. x.
40. 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.
41. Miller KM, Kaukinen KH, Beacham TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111: 237-257. doi: 10. 1023/A: 1013716020351.
42. Muirhead CA (2001) Consequences of population structure on genes under balancing selection. Evol Int J Org Evol 55: 1532-1541.
43. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous substituions. Mol Biol Evol 3: 418-426.
44. Ober C, Weitkamp LR, Cox N, Dytch H, Kostyu D, Elias S (1997) HLA and mate choice in humans. Am J Hum Genet 61: 497-504. doi: 10. 1086/515511.
45. Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B Biol Sci 270 (suppl): S254-S256. doi: 10. 1098/rsbl. 2003. 0079.
46. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153: 145-164. doi: 10. 1086/303166.
47. Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA 99: 11260-11264. doi: 10. 1073/pnas. 162006499.
48. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
49. Potts WK, Wakeland EK (1993) Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet 9: 408-412. doi: 10. 1016/0168-9525(93)90103-O.
50. Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352: 619-621. doi: 10. 1038/352619a0.
51. Reinhold K (2002) Modelling the evolution of female choice strategies under inbreeding conditions. Genetica 166: 189-195. doi: 10. 1023/A: 1021253014088.
52. Richman A (2000) Evolution of balanced genetic polymorphism. Mol Ecol 9: 1953-1963. doi: 10. 1046/j. 1365-294X. 2000. 01125. x.
53. Robinson J, Malik A, Parham P, Bodmer JG, Marsh SEG (2000) IMGT/HLA database-a sequence database for the human major histocompatibility complex. Tissue Antigens 55: 280-287. doi: 10. 1034/j. 1399-0039. 2000. 550314. x.
54. Sæther SA, Fiske P, Kålås JA (2000) Females of the lekking great snipe do not prefer males with whiter tails. Anim Behav 59: 273-280. doi: 10. 1006/anbe. 1999. 1301.
55. Sæther SA, Fiske P, Kålås JA (2001) Male mate choice, sexual conflict and strategic allocation of copulations in a lekking bird. Proc R Soc Lond B Biol Sci 268: 2097-2102. doi: 10. 1098/rspb. 2001. 1745.
56. Sæther SA, Baglo R, Fiske P, Ekblom R, Höglund J, Kålås JA (2005) Direct and indirect mate choice on leks. Am Nat 166: 145-157. doi: 10. 1086/431248.
57. Sæther SA, Fiske P, Kålås JA, Kuresoo A, Luigujõe L, Piertney SB, Sahlman T, Höglund J (2007) Inferring local adaptation from QST-FST comparisons: neutral genetic and quantitative trait variation in European populations of great snipe. J Evol Biol 20: 1563-1576. doi: 10. 1111/j. 1420-9101. 2007. 01328. x.
58. Schad J, Ganzhorn JU, Sommer S (2005) Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus. Evol Int J Org Evol 59: 439-450.
59. Schwensow N, Fietz J, Dausmann KH, Sommer S (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99: 265-277. doi: 10. 1038/sj. hdy. 6800993.
60. Slade RW, McCallum HI (1992) Overdominant vs. frequency-dependent selection at MHC loci. Genetics 123: 861-862.
61. Sommer S (2005) Major histocompatibility complex and mate choice in a monogamous rodent. Behav Ecol Sociobiol 58: 181-189. doi: 10. 1007/s00265-005-0909-7.
62. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124: 967-978.
63. Takahata N, Satta Y, Klein J (1992) Polymorphism and balancing selection at major histocompatibility complex loci. Genetics 130: 925-938.
64. Thorsby E (1997) HLA associated diseases. Hum Immunol 53: 1-11. doi: 10. 1016/S0198-8859(97)00024-4.
65. Tong JC, Bramson J, Kanduc D, Chow S, Sinha AA, Ranganathan S (2006) Modeling the bound conformation of Pemphigus Vulgaris-associated peptides to MHC Class II DR and DQ Alleles. Immunome Res 2: 1. doi: 10. 1186/1745-7580-2-1.
66. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9: 1013-1027. doi: 10. 1046/j. 1365-294x. 2000. 00964. x.
67. von Schantz T, Wittzell H, Göransson G, Grahn M, Persson K (1996) MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc R Soc Lond B Biol Sci 263: 265-271. doi: 10. 1098/rspb. 1996. 0041.
68. Wakeland EK, Boehme S, She JX, Lu CC, McIndoe RA, Cheng I, Ye Y, Potts WK (1990) Ancestral polymorphisms of MHC class II genes: divergent allele advantage. Immunol Res 9: 115-122. doi: 10. 1007/BF02918202.
69. Wedekind C, Seebeck T, Bettens F, Paepke AJ (1995) MHC-dependent mate preferences in humans. Proc R Soc Lond B Biol Sci 260: 245-249. doi: 10. 1098/rspb. 1995. 0087.
70. Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148: S469-S477. doi: 10. 1007/s10336-007-0230-5.
71. Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequences in great reed warblers: selection or drift? J Evol Biol 17: 485-492. doi: 10. 1111/j. 1420-9101. 2004. 00711. x.
72. Westerdahl H, Waldenström J, Hansson B, Hasselquist D, Bensch S (2005) An association between malaria infection and MHC in great reed warblers. Proc R Soc Lond B Biol Sci 272: 1511-1518. doi: 10. 1098/rspb. 2005. 3113.
73. Widemo F, Sæther SA (1999) Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends Ecol Evol 14: 26-31. doi: 10. 1016/S0169-5347(98)01531-6.
74. Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1999) MHC variation in birds and reptiles. Genetica 104: 301-309. doi: 10. 1023/A: 1026421607089.
75. Wu Y, Stulp RP, Ellferich P, Osinga J, Buys CHCM, Hofstra RMW (1999) Improved mutation detection in GC-rich DNA fragments by combined DGGE and CDGE. Nucleic Acids Res 27: e9. doi: 10. 1093/nar/27. 15. e9.
76. Yamazaki K, Boyse EA, Miké V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144: 1324-1335. doi: 10. 1084/jem. 144. 5. 1324.
77. Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress and prospects. Am Nat 160: S225-S237. doi: 10. 1086/342897.