Major histocompatibility complex and microsatellite variation in two populations of wild gorillas

Molecular Ecology

Volumn 13, Issue 11, 2004, Pages 3389-3402

  Lukas, D ^a,d   Bradley, B J ^a,b   Nsubuga, A M ^a   Doran Sheehy, D ^c   Robbins, M M ^a   Vigilant, L ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Demography; Gorilla; Major histocompatibility complex; Microsatellite; Noninvasive sampling; PCR errors

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; CLASSIFICATION; DNA SEQUENCE; EXON; FEMALE; GENETIC VARIABILITY; GENETICS; GORILLA; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; PHYLOGENY;

ANIMALS; EXONS; FEMALE; GORILLA GORILLA; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICROSATELLITE REPEATS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS);

GORILLA GORILLA BERINGEI; MAMMALIA; PAN (APE); PAN TROGLODYTES; PRIMATES;

EID: 7044246146     PISSN: 09621083     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2004.02353.x     Document Type: Article

References (120)

1. Alberts SC (1999) Thirteen Mhc-DQA1 alleles from two populations of baboons. Immunogenetics, 49, 825-827.
2. Avise JC (2000) Phylogeography. Harvard University Press, Cambridge MA.
3. Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annual Reviews in Genetics, 36, 19-45.
4. Beaumont MA (2003) Estimation of population growth or decline in genetically monitored populations. Genetics, 164, 1139-1160.
5. Bergström TF, Erlandsson R, Engkvist H, Josefsson A, Erlich HA, Gyllensten U (1999) Phylogenetic history of hominoid DRB loci and alleles inferred from intron sequences. Immunological Reviews, 167, 351-365.
6. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology, 16, 363-377.
7. Black FL, Hedrick PW (1997) Strong balancing selection at HLA loci: evidence from segregation in South Amerindian families. Proceedings of the National Academy of Science of the USA, 94, 12452-12456.
8. Bontrop RE, Otting N, de Groot NG, Doxiadis GG (1999) Major histocompatibility complex class II polymorphisms in primates. Immunological Reviews, 167, 339-350.
9. Boyce WM, Hedrick PW, Muggli-Cockett NE, Kalinowski S, Penedo MC, Ramey RR (1997) Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics, 145, 421-433.
10. Bradley B (2003) Molecular ecology of wild gorillas. PhD thesis, State University of New York, Stony Brook.
11. Bradley BJ, Boesch C, Vigilant L (2000) Identification and redesign of human microsatellite markers for genotyping wild chimpanzees (Pan troglodytes verus) and gorilla (Gorilla gorilla gorilla) DNA from faeces. Conservation Genetics, 1, 289-292.
12. Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L (2004) Dispersed male networks in western gorillas. Current Biology, 14, 510-513.
13. Brown JH, Jardetzky TS, Gorga JC et al. (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364, 33-39.
14. Bruford MW, Wayne RK (1993) Microsatellites and their application to population genetic studies. Current Opinion in Genetics and Development, 3, 939-943.
15. Carrington M, Nelson GW, Martin MP et al. (1999) HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science, 283, 1748-1752.
16. Clifford SL, Jeffrey K, Bruford MW, Wickings EJ (1999) Identification of polymorphic microsatellite loci in the gorilla (Gorilla gorilla gorilla) using human primers: application to noninvasively collected hair samples. Molecular Ecology, 8, 1556-1558.
17. Cohen S (2002) Strong positive selection and habitat-specific amino acid substitution patterns in MHC from an estuarine fish under intense pollution stress. Molecular Biology and Evolution, 19, 1870-1880.
18. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution, 53, 1259-1267.
19. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution, 15, 290-295.
20. Doherty PC, Zinkernagel RM (1975) A biological role for the major histocompatibility antigens. Lancet, 1, 1406-1409.
21. Dorak MT, Lawson T, Machulla HK, Mills KI, Burnett AK (2002) Increased heterozygosity for MHC class II lineages in newborn males. Genes and Immunity, 3, 263-269.
22. Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah N (2002) Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. American Journal of Primatology, 58, 91-116.
23. Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends in Genetics, 16, 551-558.
24. Evermann JF, Heeney JL, Roelke ME, McKeirnan AJ, O'Brien SJ (1988) Biological and pathological consequences of feline infectious peritonitis virus infection in the cheetah. Archives of Virology, 102, 155-171.
25. Fabiani A, Hoelzel AR, Galimberti F, Muelbert MM (2003) Long-range paternal gene flow in the southern elephant seal. Science, 299, 676.
26. Fattorini P, Cossutta F, Giulianini P, Edomi P, Previdere C (2000) DNA damage promotes mistyping in the allele specific oligonucleotide probing analysis of forensic samples. Electrophoresis, 21, 2969-2972.
27. Garner KJ, Ryder OA (1996) Mitochondrial DNA diversity in gorillas. Molecular Phylogenetics and Evolution, 6, 39-48.
28. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution, 57, 1707-1722.
29. Go Y, Satta Y, Kawamoto Y, Rakotoarisoa G, Randrianjafy A, Koyama N, Hirai H (2002) Mhc-DRB genes evolution in lemurs. Immunogenetics, 54, 403-417.
30. Groves CP (2001) Primate Taxonomy, 1st edn. Smithsonian Institution Press, Washington.
31. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361-372.
32. Gutierrez-Espeleta GA, Hedrick PW, Kalinowski ST, Garrigan D, Boyce WM (2001) Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity, 86, 439-450.
33. Gyllensten U, Sundvall M, Ezcurra I, Erlich HA (1991a) Genetic diversity at class II DRB loci of the primate MHC. Journal of Immunology, 146, 4368-4376.
34. Gyllensten UB, Sundvall M, Erlich HA (1991b) Allelic diversity is generated by intraexon sequence exchange at the DRB1 locus of primates. Proceedings of the National Academy of Science of the USA, 88, 3686-3690.
35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
36. Hambuch TM, Lacey EA (2002) Enhanced selection for MHC diversity in social tuco-tucos. Evolution, 56, 841-845.
37. Harcourt A (1996) Is the gorilla a threatened species? How should we judge? Biological Conservation, 75, 165-176.
38. Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics, 104, 449-456.
39. Hedrick PW, Miller PS (1991) MHC polymorphism and the design of captive breeding programs - simple solutions are not the answer. Conservation Biology, 5, 556-558.
40. Hedrick PW, Parker KM, Miller EL, Miller PS (1999) Major histocompatibility complex variation in the endangered Przewalski's horse. Genetics, 152, 1701-1710.
41. Hedrick PW, Parker KM, Gutierrez-Espeleta GA, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian oryx. Evolution, 54, 2145-2151.
42. Hedrick PW, Gutierrez-Espeleta GA, Lee RN (2001) Founder effect in an island population of bighorn sheep. Molecular Ecology, 10, 851-857.
43. Hedrick PW, Lee RN, Garrigan D (2002) Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Molecular Ecology, 11, 1905-1913.
44. Hill AV (1999) The immunogenetics of resistance to malaria. Proceedings of the Association of American Physicians, 111, 272-277.
45. Hill AV, Allsopp CE, Kwiatkowski D et al. (1991) Common west African HLA antigens are associated with protection from severe malaria. Nature, 352, 595-600.
46. Hoelzel AR, Stephens JC, O'Brien SJ (1999) Molecular genetic diversity and evolution at the MHC DQB locus in four species of pinnipeds. Molecular Biology and Evolution, 16, 611-618.
47. Höss M, Kohn M, Pääbo S, Knauer F, Schröder W (1992) Excrement analysis by PCR. Nature, 359, 199.
48. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proceedings of the National Academy of Science of the USA, 86, 958-962.
49. Hurley CK, Fernandez-Vina M, Middleton D et al. (2001) Chapter 2c: Class II HLA-typing: primers and probes. In: IHWG Technical Manual Genomic Analysis of the Human MHC: DNA-Based Typing for HLA Alleles and Linked Polymorphisms (ed. International Histocompatibility Working Group). http://www.ihwg.org/tmanual/2c. pdf.
50. Jensen-Seaman MI (2000) Evolutionary genetics of gorillas. PhD thesis, Yale University, New Haven.
51. Jensen-Seaman MI, Kidd KK (2001) Mitochondrial DNA variation and biogeography of eastern gorillas. Molecular Ecology, 10, 2241-2247.
52. Jensen-Seaman MI, Deinard AS, Kidd KK (2003) Mitochondrial and nuclear DNA estimates of divergence between western and eastern gorillas. In: Gorilla Biology (eds Taylor AB, Goldsmith ML), pp. 247-268. Cambridge University Press, Cambridge MA.
53. Jepson A, Banya W, Sisay-Joof F et al. (1997) Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Infection and Immunity, 65, 872-876.
54. Judo MS, Wedel AB, Wilson C (1998) Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Research, 26, 1819-1825.
55. Kaessmann H, Wiebe V, Weiss G, Pääbo S (2001) Great ape DNA sequences reveal a reduced diversity and an expansion in humans. Nature Genetics, 27, 155-156.
56. Kalpers J, Williamson EA, Robbins MM et al. (2003) Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx, 37, 326-337.
57. Kasahara M, Klein D, Vincek V, Sarapata DE, Klein J (1992) Comparative anatomy of the primate major histocompatibility complex DR subregion: evidence for combinations of DRB genes conserved across species. Genomics, 14, 340-349.
58. Kenter M, Otting N, Anholts J, Jonker M, Schipper R, Bontrop RE (1992) Mhc-DRB diversity of the chimpanzee (Pan troglodytes). Immunogenetics, 37, 1-11.
59. Kenter M, Otting N, de Weers M et al. (1993) Mhc-DRB and -DQA1 nucleotide sequences of three lowland gorillas. Implications for the evolution of primate Mhc class II haplotypes. Human Immunology, 36, 205-218.
60. Kilger C, Krings M, Poinar H, Pääbo S (1997) Colony sequencing: direct sequencing of plasmid DNA from bacterial colonies. Biotechniques, 22, 412-418.
61. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
62. Klein J (1989) The MHC trans-species hypothesis: in the discussion period. Immunology Supplement, 2, 36-39.
63. Klein J, Bontrop RE, Dawkins RL et al. (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics, 31, 217-219.
64. Klein J, O'hUigin C, Figueroa F, Mayer WE, Klein D (1993) Different modes of MHC evolution in primates. Molecular Biology and Evolution, 10, 48-59.
65. Knapp LA, Ha JC, Sackett GP (1996) Parental MHC antigen sharing and pregnancy wastage in captive pigtailed macaques. Journal of Reproduction and Immunology, 32, 73-88.
66. Kobayashi N, Tamura K, Aotsuka T (1999) PCR error and molecular population genetics. Biochemical Genetics, 37, 317-321.
67. Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature, 419, 826-830.
68. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics, 17, 1244-1245.
69. Kupfermann H, Mayer WE, O'hUigin C, Klein D, Klein J (1992) Shared polymorphism between gorilla and human major histocompatibility complex DRB loci. Human Immunology, 34, 267-278.
70. Lafferty K, Gerber LR (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conservation Biology, 16, 1-12.
71. Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Molecular Ecology, 10, 2525-2539.
72. Larson S, Jameson R, Etnier M, Fleming M, Bentzen P (2002) Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries. Molecular Ecology, 11, 1899-1903.
73. Longeri M, Zanotti M, Damiani G (2002) Recombinant DRB sequences produced by mismatch repair of heteroduplexes during cloning in Escherichia coli. European Journal of Immunogenetics, 29, 517-523.
74. Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics, 151, 1211-1216.
75. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Molecular Ecology, 7, 963-974.
76. Lyles AM, Dobson AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine, 24, 315-326.
77. Mackiewicz M, Fletcher DB, Wilkins SD, DeWoody JA, Avise JC (2002) A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Molecular Ecology, 11, 1877-1883.
78. Maudet C, Miller C, Bassano B et al. (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Molecular Ecology, 11, 421-436.
79. McNeilage A, Plumptre AJ, Brock-Doyle A, Vedder A (2001) Bwindi Impenetrable National Park, Uganda: gorilla census 1997. Oryx, 35, 39-47.
80. Meyerhans A, Vartanian JP, Wain-Hobson S (1990) DNA recombination during PCR. Nucleic Acids Research, 18, 1687-1691.
81. Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution, 17, 551-557.
82. Mikko S, Roed K, Schmutz S, Andersson L (1999) Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants. Immunological Reviews, 167, 169-178.
83. Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, Woodruff DS (1994) Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science, 265, 1193-1201.
84. Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Molecular Ecology, 10, 1835-1844.
85. Murray DL, Kapke CA, Evermann JF, Fuller TK (1999) Infectious disease and the conservation of free-ranging large carnivores. Animal Conservation, 2, 241-254.
86. Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York.
87. Nino-Vasquez JJ, Vogel D, Rodriguez R et al. (2000) Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites. Immunogenetics, 51, 219-230.
88. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology, 13, 2089-2094.
89. Pääbo S, Irwin DM, Wilson AC (1990) DNA damage promotes jumping between templates during enzymatic amplification. Journal of Biological Chemistry, 265, 4718-4721.
90. Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics, 147, 1943-1957.
91. Raymond M, Rousset F (1995) GENEPOP Version 1.2.: population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
92. Richman AD, Herrera LG, Nash D (2003) Evolution of MHC class II Eβ diversity within the genus Peromyscus. Genetics, 164, 289-297.
93. Robbins MM, McNeilage A (2003) Home range and frugivory patterns of mountain gorillas in Bwindi Impenetrable National Park, Uganda. International Journal of Primatology, 24, 467-491.
94. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genetics, 35, 103-106.
95. Robinson J, Waller MJ, Parham P et al. (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Research, 31, 311-314.
96. Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics, 140, 1413-1419.
97. Saiki RK, Gelfand DH, Stoffel S et al. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science, 239, 487-491.
98. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425.
99. Sauermann U, Nürnberg P, Bercovitch FB et al. (2001) Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques. Human Genetics, 108, 249-254.
100. Scharf SJ, Long CM, Erlich HA (1988) Sequence analysis of the HLA DR beta and HLA DQ beta loci from three Pemphigus vulgaris patients. Human Immunology, 22, 61-69.
101. Seddon JM, Baverstock PR (1999) Variation on islands: major histocompatibility complex (MHC) polymorphism in populations of the Australian bush rat. Molecular Ecology, 8, 2071-2079.
102. Slate J, Kruuk LE, Marshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proceedings of the Royal Society of London, Series B, 267, 1657-1662.
103. Smulders MJM, Snoek LB, Booy G, Vosman B (2003) Complete loss of MHC genetic diversity in the common hamster (Cricetus cricetus) population in the Netherlands: consequences for conservation strategies. Conservation Genetics, 4, 441-451.
104. Taberlet P, Griffin S, Goossens B et al. (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research, 24, 3189-3194.
105. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends in Ecology and Evolution, 14, 323-327.
106. Thalmann O, Hebler J, Poinar HN, Pääbo S, Vigilant L (2004) Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Molecular Ecology, 13, 321-335.
107. Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucleic Acids Research, 30, 2083-2088.
108. Thursz M, Yallop R, Goldin R, Trepo C, Thomas HC (1999) Influence of MHC class II genotype on outcome of infection with hepatitis C virus. The HENCORE group. Hepatitis C European Network for Cooperative Research. Lancet, 354, 2119-2124.
109. van Tienderen PH, de Haan AA, van der Linden G, Vosman B (2002) Biodiversity assessment using markers for ecologically important traits. Trends in Ecology and Evolution, 17, 577-582.
110. Titus-Trachtenberg EA, Rickards O, De Stefano GF, Erlich HA (1994) Analysis of HLA class II haplotypes in the Cayapa Indians of Ecuador: a novel DRB1 allele reveals evidence for convergent evolution and balancing selection at position 86. American Journal of Human Genetics, 55, 160-167.
111. Vigilant L (2002) Technical challenges in the microsatellite genotyping of a wild chimpanzee population using feces. Evolutionary Anthropology, 11, 162-165.
112. Vigilant L, Bradley B (2004) Genetic variation in gorillas. American Journal of Primatology, 64, 161-172.
113. Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proceedings of the National Academy of Science of the USA, 98, 12890-12895.
114. Vogel TU, Evans DT, Urvater JA, O'Connor DH, Hughes AL, Watkins DI (1999) Major histocompatibility complex class I genes in primates: co-evolution with pathogens. Immunological Reviews, 167, 327-337.
115. Walsh PD, Abernethy KA, Bermejo M et al. (2003) Catastrophic ape decline in western equatorial Africa. Nature, 422, 611-614.
116. van der Walt JM, Nel LH, Hoelzel AR (2001) Characterization of major histocompatibility complex DRB diversity in the endemic South African antelope Damaliscus pygargus: a comparison in two subspecies with different demographic histories. Molecular Ecology, 10, 1679-1688.
117. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. Journal of Evolutionary Biology, 16, 224-232.
118. Wenink PW, Groen AF, Roelke-Parker ME, Prins HH (1998) African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Molecular Ecology, 7, 1315-1322.
119. Yu N, Jensen-Seaman MI, Chemnick L, Ryder O, Li WH (2004) Nucleotide diversity in gorillas. Genetics, 166, 1375-1388.
120. Zylstra P, Rothenfluh HS, Weiller GF, Blanden RV, Steele EJ (1998) PCR amplification of murine immunoglobulin germline V genes: strategies for minimization of recombination artefacts. Immunology and Cell Biology, 76, 395-405.