Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation

Journal of Evolutionary Biology

Volumn 24, Issue 9, 2011, Pages 1847-1856

  Eimes, J A ^a   Bollmer, J L ^a   Whittingham, L A ^a   Johnson, J A ^b   Van Oosterhout, C ^c   Dunn, P O ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^b UNIVERSITY OF NORTH TEXAS   (United States)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Bottleneck; Copy number variation; Genetic drift; Major histocompatibility complex; Selection; Tympanuchus cupido

Indexed keywords

ALLELE; DISEASE RESISTANCE; EXTINCTION; FITNESS; GENETIC DRIFT; GENETIC MARKER; GENETIC VARIATION; IMMUNITY; NUMERICAL MODEL; POPULATION BOTTLENECK; POPULATION DECLINE; POULTRY; PRAIRIE; RISK FACTOR; SELECTION;

ALLELE; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; COPY NUMBER VARIATION; GALLIFORMES; GENE; GENETIC DRIFT; GENETICS; MOLECULAR GENETICS; POPULATION GENETICS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; COMPUTER SIMULATION; DNA COPY NUMBER VARIATIONS; GALLIFORMES; GENES, MHC CLASS II; GENETIC DRIFT; GENETICS, POPULATION; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH;

UNITED STATES; WISCONSIN;

TYMPANUCHUS CUPIDO; VERTEBRATA;

EID: 80051669124     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02311.x     Document Type: Article

References (66)

1. Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D. & Wayne, R.K. 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl Acad. Sci. USA 101: 3490-3494.
2. Aldhous, M.C., Abu Bakar, S., Prescott, N.J. et al. 2010. Measurement methods and accuracy in copy number variation: failure to replicate associations of beta-defensin copy number with Crohn's disease. Hum. Mol. Genet. 19: 4930-4938.
3. Anderson, R.K. & Toepfer, J.E. 1999. History, status and management of the greater prairie chicken in Wisconsin. In: The Greater Prairie Chicken, a National Look (W.D. Svedarsky, R.H. Hier & N.J. Silvy, eds), pp. 39-57. Minnesota Agricultural Experiment Station, University of Minnesota, St. Paul.
4. Anmarkrud, J.A., Johnsen, A., Bachmann, L. & Lifjeld, J.T. 2010. Ancestral polymorphism in exon 2 of bluethroat (Luscinia svecica) MHC class II B genes. J. Evol. Biol. 23: 1206-1217.
5. 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.
6. Babik, W., Pabijan, M., Arntzen, J.W. et al. 2009. Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol. Ecol. 18: 769-781.
7. Balakrishnan, C., Ekblom, R., Volker, M., Westerdahl, H., Godinez, R., Kotkiwicz, H. et al. 2010. Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol. 8: doi.
8. Bellinger, R., Johnson, J., Toepfer, J. & Dunn, P.O. 2003. Loss of genetic variation in greater prairie chickens following a population bottleneck in Wisconsin, USA. Conserv. Biol. 17: 717-724.
9. Borghans, J.A.M., Beltman, J.B. & De Boer, R.J. 2004. MHC polymorphism under host-pathogen coevolution. Immunogenetics 55: 732-739.
10. Briles, W.E., Briles, R.W., Taffs, R.E. & Stone, H.A. 1983. Resistance to a malignant lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science 219: 977-979.
11. Brown, J.H., Jardetzky, T.S., Gorga, J.C. et al. 1993. 3-dimensional structure of the human class-II histocompatibility antigen HLA-Dr1. Nature 364: 33-39.
12. Bryant, D. & Moulton, V. 2002. NeighborNet: an agglomerative method for the construction of planar phylogenetic networks. doi.
13. Cahan, P. & Graubert, T.A. 2010. Integrated genomics of susceptibility to alkylator-induced leukemia in mice. BMC Genomics 11: doi.
14. Chaves, L.D., Faile, G.M., Krueth, S.B., Hendrickson, J.A. & Reed, K.M. 2010. Haplotype variation, recombination, and gene conversion within the turkey MHC-B locus. Immunogenetics 62: 465-477.
15. Crow, F. & Kimura, A. 1970. An Introduction to Population Genetics Theory. Harper and Row, New York.
16. Cummings, S., McMullan, M., Joyce, D. & van Oosterhout, C. 2010. Solutions for PCR, cloning and sequencing errors in population genetic analysis. Conserv. Genet. 11: 1095-1097.
17. Cutler, G., Marshall, L.A., Chin, N., Baribault, H. & Kassner, P.D. 2007. Significant gene content variation characterizes the genomes of inbred mouse strains. Genome Res. 17: 1743-1754.
18. Doxiadis, G.G.M., de Groot, N., de Groot, N.G. et al. 2010. Extensive DRB region diversity in cynomolgus macaques: recombination as a driving force. Immunogenetics 62: 137-147.
19. Eimes, J.A., Bollmer, J.L., Dunn, P.O., Whittingham, L.A. & Wimpee, C. 2010. Mhc class II diversity and balancing selection in greater prairie-chickens. Genetica 138: 265-271.
20. Ejsmond, M.J. & Radwan, J. 2011. MHC diverstity in bottlenecked populations: a simulation model. Conserv. Genet. 12: 129-137.
21. Garrigan, D. & Hedrick, P.W. 2003. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57: 1707-1722.
22. Hall, T.A. 1999. Bioedit is a user friendly sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
23. Hansen, A., Willerslev, E., Wiuf, C., Mourier, T. & Arctander, P. 2001. Statistical evidence for miscoding lesions in ancient DNA templates. Mol. Biol. Evol. 18: 262-275.
24. Hedrick, P.W. 2001. Conservation genetics: where are we now? Trends Ecol. Evol. 16: 629-636.
25. Hedrick, P.W. 2003. The major histocompatibility complex (MHC) in declining populations: an example of adaptive variation. In: Reproduction Science and Integrated Conservation (W. Holt, A. Pickard, J. Rodger & D. Wildt, eds), pp. 97-113. Cambridge University Press, Cambridge.
26. Hedrick, P.W., Parker, K.M., Gutierrez-Espeleta, G.A., Rattink, A. & Lievers, K. 2000. Major histocompatibility complex variation in the Arabian oryx. Evolution 54: 2145-2151.
27. Hedrick, P.W., Lee, R.N. & Garrigan, D. 2002. Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Mol. Ecol. 11: 1905-1913.
28. Hosomichi, K., Shiina, T., Suzuki, S. et al. 2006. The major histocompatibility complex (Mhc) class IIB region has greater genomic structural flexibility and diversity in the quail than the chicken. BMC Genomics 7: doi.
29. Huson, D.H. & Bryant, D. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23: 254-267.
30. Johnsgard, P.A. 2002. Grassland Grouse. Smithsonian Institution Press, Washington, DC.
31. Johnson, J.A., Toepfer, J. & Dunn, P.O. 2003. Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens. Mol. Ecol. 12: 3335-3347.
32. Johnson, J.A., Bellinger, R., Toepfer, J. & Dunn, P.O. 2004. Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol. Ecol. 13: 2617-2630.
33. Johnson, J.A., Dunn, P.O. & Bouzat, J.L. 2007. Effects of recent population bottlenecks on reconstructing the demographic history of prairie-chickens. Mol. Ecol. 16: 2203-2222.
34. Johnson, J., Schroeder, M. & Robb, L. 2011. Greater prairie-chicken (Tympanuchus cupido). In: The Birds of North America. (Poole, E. ed.). Cornell Lab of Ornithology, Ithaca, New York.
35. Kelley, J., Walter, L. & Trowsdale, J. 2005. Comparative genomics of major histocompatibility complexes. Immunogenetics 56: 683-695.
36. Klein, J. 1986. The Natural History of the Major Histocompatibility Complex. John Wiley, New York.
37. Klein, J., Ono, H., Klein, D. & O'hUigin, C. 1993. The accordian model of MHC evolution. Prog. Immunol. 8: 137-143.
38. Langefors, K., Lohm, J. & von Schantz, T. 2001. Allelic polymorphism in MHC class IIB in four populations of Atlantic salmon (Salmo salar). Immunogenetics 53: 329-336.
39. Le Corre, V. & Kremer, A. 2003. Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164: 1205-1219.
40. McMullan, M. 2010. Host-parasite Co-evolution and Genetic Variation at the Major Histocompatibility Complex (MHC) in the Guppy, Poecilia reticulata. PhD Thesis, University of Hull, UK.
41. Miller, H.C. & Lambert, D.M. 2004. Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol. Ecol. 13: 3709-3721.
42. Mona, S., Crestanello, B., Bankhead-Dronnet, S. et al. 2008. Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Mol. Ecol. 17: 4053-4067.
43. Nei, M. 2005. Bottlenecks, genetic polymorphism and speciation. Genetics 170: 1-4.
44. Nei, M. & Gojobori, T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
45. Nei, M., Gu, X. & Sitnikova, T. 1997. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc. Natl Acad. Sci. USA 94: 7799-7806.
46. Nozawa, M., Kawahara, Y. & Nei, M. 2007. Genomic drift and copy number variation of sensory receptor genes in humans. Proc. Natl Acad. Sci. USA 104: 20421-20426.
47. van Oosterhout, C. 2009. A new theory of MHC evolution: beyond selection on the immune genes. Proc. Biol. Sci. 276: 657-665.
48. van Oosterhout, C., Joyce, D.A., Cummings, S.M. et al. 2006a. Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60: 2562-2574.
49. van Oosterhout, C., Joyce, D.A. & Cummings, S.M. 2006b. Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97: 111-118.
50. Paabo, S., Poinar, H., Serre, D. et al. 2004. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38: 645-679.
51. Piertney, S.B. & Oliver, M.K. 2006. The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
52. Potts, W.K. & Wakeland, E.K. 1990. Evolution of diversity at the major histocompatibility complex. Trends Ecol. Evol. 5: 181-187.
53. Radwan, J., Biedrzycka, A. & Babik, W. 2010. Does reduced MHC diversity decrease viability of vertebrate populations? Biol. Conserv. 143: 537-544.
54. Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
55. Schad, J., Ganzhorn, J.U. & Sommer, S. 2005. Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus. Evolution 59: 439-450.
56. Schrider, D.R. & Hahn, M.W. 2010. Gene copy-number polymorphism in nature. Proc. Biol. Sci. 277: 3213-3221.
57. Sefc, K.M., Payne, R.B. & Sorenson, M.D. 2007. Single base errors in PCR products from avian museum specimens and their effect on estimates of historical genetic diversity. Conserv. Genet. 8: 879-884.
58. Shiina, T., Ota, M., Shimizu, S. et al. 2006. Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173: 1555-1570.
59. Siddle, H.V., Kreiss, A., Eldridge, M.D.B. et al. 2007. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc. Natl Acad. Sci. USA 104: 16221-16226.
60. Siddle, H.V., Marzec, J., Cheng, Y., Jones, M. & Belov, K. 2010. MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. Proc. Biol. Sci. 277: 2001-2006.
61. Sommer, S. 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front. Zool. 2: 1-18.
62. Spurgin, L. & Richardson, D. 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. Biol. Sci. 277: 979-988.
63. Strand, T., Westerdahl, H., Hoeglund, J., Alatalo, R.V. & Siitari, H. 2007. The Mhc class II of the black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression. Immunogenetics 59: 725-734.
64. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
65. Trowsdale, J. 1995. Both man and bird and beast - comparative organization of mhc genes. Immunogenetics 41: 1-17.
66. Ye, Z.Q., Niu, S., Yu, Y. et al. 2010. Analyses of copy number variation of GK rat reveal new putative type 2 diabetes susceptibility loci. PLoS ONE 5: doi.