The Major Histocompatibility Complex and Primate Behavioral Ecology: New Tools and Future Questions

International Journal of Primatology

Volumn 35, Issue 1, 2014, Pages 11-31

  Huchard, Elise ^a   Pechouskova, Eva ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GERMAN PRIMATE CENTER   (Germany)

Author keywords

Kin discrimination; major histocompatibility complex; mate choice; MHC genotyping; next generation sequencing; primates; sexual behavior

Indexed keywords

EID: 84893723745     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-013-9700-1     Document Type: Article

References (103)

1. Aksenov, A. A., Gojova, A., Zhao, W., Morgan, J. T., Sankaran, S., Sandrock, C., et al. (2012). Characterization of volatile organic compounds in human leukocyte antigen heterologous expression systems: A cell's "chemical odor fingerprint". Chembiochem, 13, 1053-1059.
2. Alberts, B. (2002). Isolating, cloning and sequencing DNA. In B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, & P. Walter (Eds.), Molecular biology of the cell (4th ed.). New York: Garland.
3. Alberts, S. C., & Ober, C. (1993). Genetic variability in the major histocompatibility complex: a review of non-pathogen-mediated selective mechanisms. Yearbook of Physical Anthropology, 36, 71-89.
4. Alvergne, A., Huchard, E., Caillaud, D., Charpentier, M. J. E., Setchell, J. M., Ruppli, C., Féjan, D., Martinez, L., Cowlishaw, G., & Raymond, M. (2009). Human ability to recognize kin visually within primates. International Journal of Primatology, 30, 199-210.
5. Apanius, V., Penn, D., Slev, P., Ruff, L. R., & Potts, W. K. (1997). The nature of selection on the major histocompatibility complex. Critical Review of Immunology, 17, 179-224.
6. Babik, W. (2010). Methods for MHC genotyping in non-model vertebrates. Molecular Ecology Resources, 10, 237-251.
7. Babik, W., Taberlet, P., Ejsmond, M. J., & Radwan, J. (2009). New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Molecular Ecology Resources, 9(3), 713-719.
8. Balloux, F., Amos, W., & Coulson, T. (2004). Does heterozygosity estimate inbreeding in real populations? Molecular Ecology, 13(10), 3021-3031.
9. 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.
10. Blais, J., Rico, C., van Oosterhout, C., Cable, J., Turner, G. F., & Bernatchez, L. (2007). MHC adaptive divergence between closely related and sympatric African Cichlids. PloS One, 8, 1-12.
11. Brown, J. L., & Eklund, A. (1994). Kin recognition and the major histocompatibility complex-an integrative review. American Naturalist, 143(3), 435-461.
12. Célerier, A., Huchard, E., Alvergne, A., Féjan, D., Plard, F., Cowlishaw, G., Raymond, M., & Bonnadona, F. (2010). Detective mice assess relatedness in baboons using olfactory cues. Journal of Experimental Biology, 213, 1399-1405.
13. Chaix, R., Cao, C., & Donelly, P. (2008). Is mate choice in humans MHC-Dependent? PLoS Genetics, 4, 1-5.
14. Charpentier, M., Crawford, J., Boulet, M., & Drea, C. (2010). Lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Animal Behaviour, 80, 101-108.
15. Charpentier, M. J. E., Boulet, M., & Drea, C. M. (2008). Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Molecular Ecology, 17, 3225-3233.
16. Cheetham, S. A., Thom, M. D., Jury, F., Ollier, W. E. R., Beynon, R. J., & Hurst, J. L. (2007). The genetic basis of individual-recognition signals in the mouse. Current Biology, 17, 1771-1777.
17. Cowlishaw, G., & Dunbar. (1991). Dominance rank and mating success in male primates. Animal Behaviour, 41, 1045-1056.
18. de Groot, N. G., Otting, N., Doxiadis, G. G., Balla-Jhagjhoorsingh, S. S., Heener, J. L., van Rood, J. J., Gagneux, P., & Bontrop, R. E. (2002). Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proceedings of the National Academy of Sciences of the United States, 99, 11748-11753.
19. de Groot, N., Doxiadis, G. G., de Vos-Rouweler, A. J., de Groot, N. G., Verschoor, E. J., & Bontrop, R. E. (2008). Comparative genetics of a highly divergent DRB microsatellite in different macaque species. Immunogenetics, 60, 737-748.
20. Dixson, A. F. (1998). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press.
21. Doherty, P. C., & Zinkernagel, R. M. (1975). Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature, 256, 50-52.
22. Doxiadis, G. G., De Groot, N., Claas, F. H. J., Doxiadis, I. I. N., van Rood, J. J., & Bontrop, R. E. (2007). A highly divergent microsatellite facilitating fast and accurate DRB haplotyping in humans and rhesus macaques. Proceedings of the National Academy of Sciences of the USA, 104, 8907-8912.
23. Ehlers, A., Beck, S., Forbes, S., Trowsdale, J., Uchanska-Ziegler, B., Volz, A., Younger, R., & Ziegler, A. (2000). MHC-Linked olfactory receptor loci exhibit polymorphism and contribute to extended HLA/OR-haplotypes. Genome Research, 10, 1968-1978.
24. Eizaguirre, C., Lenz, T. L., Kalbe, M., & Milinski, M. (2012). Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field. Ecology Letters, 15, 723-731.
25. Eizaguirre, C., Lenz, T. L., Traulsen, A., & Milinski, M. (2009a). Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecology Letters, 12, 5-12.
26. Eizaguirre, C., Yeates, S. E., Lenz, T. L., Kalbe, M., & Milinski, M. (2009b). MHC-based mate choice combines good genes and maintenance of MHC polymorphism. Molecular Ecology, 18, 3316-3329.
27. Galan, M., Guivier, E., Caraux, G., Charbonnel, N., & Cosson, J.-F. (2010). A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics, 11, 296.
28. Gavrilets, S. (2004). Fitness landscapes and the origin of species. Princeton, NJ: Princeton University Press.
29. Gowaty, P. A. (2004). Sex roles, contests for the control of reproduction, and sexual selection. In P. K. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 37-54). Cambridge, U. K.: Cambridge University Press.
30. Havlicek, J., & Roberts, C. (2009). MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology, 34, 497-512.
31. Heymann, E. W. (2006). The neglected sense of smell in primate behavior, ecology and evolution. American Journal of Primatology, 68, 514-524.
32. Horton, R., Wilming, L., Rand, V., Lovering, R. C., Bruford, E. A., Khodiyar, V. K., Lush, M. J., Povey, S., Talbot, C. C., Wright, M. W., Wain, H. M., Trowsdale, J., Ziegler, A., & Beck, S. (2004). Gene map of the extended human MHC. Nature Reviews Genetics, 5, 889-899.
33. Hoskin, C. J., & Higgie, M. (2010). Speciation via species interactions: the divergence of mating traits within species. Ecology Letters, 13, 409-420.
34. Huchard, E., Albrecht, C., Schliehe-Diecks, S., Baniel, A., Roos, C., Kappeler, P., & Brameier, M. (2012). Large-scale MHC class II genotyping of a wild lemur population by next generation sequencing. Immunogenetics, 64(12), 895-913.
35. Huchard, E., Baniel, A., Schliehe-Diecks, S., & Kappeler, P. M. (2013). MHC-disassortative mate choice and inbreeding avoidance in a solitary primate. Molecular Ecology, 22, 4071-4086.
36. Huchard, E., Cowlishaw, G., Raymond, M., Weill, M., & Knapp, L. A. (2006). Molecular study of Mhc-DRB in wild chacma baboons reveals high variability and evidence for trans-species inheritance. Immunogenetics, 58(10), 805-816.
37. Huchard, E., Knapp, L. A., Wang, J., Raymond, M., & Cowlishaw, G. (2010a). MHC, mate choice and heterozygote advantage in a wild social primate. Molecular Ecology, 19, 2545-2561.
38. Huchard, E., Raymond, M., Benavides, J., Marshall, H., Knapp, L. A., & Cowlishaw, G. (2010b). A female signal reflects MHC genotype in a social primate. BMC Evolutionary Biology, 10, 10.
39. Huchard, E., Weill, M., Cowlishaw, G., Raymond, M., & Knapp, L. A. (2008). Polymorphism, haplotype composition, and selection in the Mhc-DRB of wild baboons. Immunogenetics, 60, 585-598.
40. Hughes, A. L., & Yeager, M. (1998). Natural selection at major histocompatibility complex loci of vertebrates. Annual Review of Genetics, 32, 415-432.
41. Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A., & Beynon, R. J. (2001). Individual recognition in mice mediated by major urinary proteins. Nature, 414, 631-634.
42. Hurst, J. L., Thom, M. D., Nevison, C. M., Humphries, R. E., & Beynon, R. J. (2005). MHC odours and not required or sufficient for recognition of individuals scent owners. Proceedings of the Royal Society of London B: Biological Sciences, 272, 715-724.
43. Janeway, C., Travers, P., Walport, M., & Shlombick, M. (2005). Immunobiology: The immune system in health and disease (6th ed.). New York: Garland.
44. Kappeler, P. M. (2002). Sexual selection in primates: new and comparative perspectives. Evolutionary Anthropology, 11, 173-175.
45. Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707-740.
46. Kappeler, P. M., & Watts, D. P. (Eds.). (2012). Long-term field studies of primates. Heidelberg: Springer.
47. Kazem, A., & Widdig, A. (2013). Visual phenotype matching: cues to paternity are present in rhesus macaque faces. PloS One, 8, e55846.
48. Kessler, S. E., Scheumann, M., Nash, L. T., & Zimmerman, E. (2012). Paternal kin recognition in the high frequency/ultrasonic range in a solitary foraging mammal. BMC Ecology, 12, 26.
49. Knapp, L. A. (2005a). The ABC'S of MHC. Evolutionary Anthropology, 14, 28-37.
50. Knapp, L. A. (2005b). Denaturating gradient gel electrophoresis and its use in the detection of major histocompatibility complex polymorphisms. Tissue Antigens, 65, 211-219.
51. Knapp, L. A. (2007). Selection on MHC: a matter of form over function. Heredity, 99, 241-242.
52. Knapp, L. A., Cadavid, L. F., Eberle, M. E., Knechtle, S. J., Bontrop, R. E., & Watkins, D. I. (1997). Identification of new Mamu-DRB alleles using DGGE and direct sequencing. Immunogenetics, 45, 171-179.
53. Kwak, J., Willse, A., Matsumura, K., Opiekun, M. C., Yi, W., Preti, G., Yamazaki, K., & Beauchamp, G. K. (2008). Genetically-based olfactory signatures persist despite dietary variation. PloS One, 3, 10.
54. Kwak, J., Willse, A., Preti, G., Yamazaki, K., & Bauchamp, G. K. (2011). In search of the chemical basis for MHC odourtypes. Proceedings of the Royal Society of London B: Biological Sciences, 277, 2417-2425.
55. Laurent, R., & Chaix, R. (2012). MHC-dependent mate choice in humans: why genomic patterns from the HapMap European American dataset support the hypothesis. BioEssays, 34, 267-271.
56. Leinders-Zufall, T., Brennan, P., Widmayer, P., Chandramani, P., Maul-Pavicic, A., Jager, M., Li, X. H., Breer, H., Zufall, F., & Boehm, T. (2004). MHC class I peptides as chemosensory signals in the vomeronasal organ. Science, 306(5698), 1033-1037.
57. Logan, D. W., Marton, T. F., & Stowers, L. (2008). Species specificity in major urinary proteins by parallel evolution. PloS One, 3, e3280.
58. Lukas, D., Bradley, B. J., Nsubuga, A. M., Doran-Sheehy, D., Robbins, M. M., & Vigilant, L. (2004). Major histocompatibility complex and microsatellite variation in two populations of wild gorillas. Molecular Ecology, 13, 3389-3402.
59. Metzker, M. L. (2010). Sequencing technologies-the next generation. Nature Reviews Genetics, 11, 31-46.
60. Milinski, M. (2006). The major histocompatibility complex, sexual selection, and mate choice. Annual Review of Ecology, Evolution, and Systematics, 37, 159-186.
61. Milinski, M., Croy, I., Hummel, T., & Boehm, T. (2013). Major histocompatibility complex peptide ligands as olfactory cues in human body odour assessment. Proceedings of the Royal Society B, 280, 20122889.
62. Mitani, J. C., Call, J., Kappeler, P. M., Palombit, R. A., & Silk, J. B. (Eds.). (2012). The evolution of primate societies. Chicago: University of Chicago Press.
63. Myers, R. M., Fischer, S. G., Lerman, L. S., & Maniatis, T. (1987). Nearly all single base substitutions in DNA fragments joined to GC-clamp can be detected by denaturing gradient gel electrophoresis. Nucleic Acids Research, 13, 3131-3145.
64. Orita, M., Iwahana, H., Kanazawa, H., Hayashi, K., & Sekiya, T. (1989). Detection of polymorphism of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proceedings of the National Academy of Sciences of the USA, 86, 2766-2770.
65. Otting, N., Heijmans, C. M. C., Noort, R. C., de Groot, N. G., Doxiadis, G. G. M., van Rood, J. J., Watkins, D. I., & Bontrop, R. E. (2005). Unparalleled complexity of the MHC class I region in rhesus macaques. Proceedings of the National Academy of Sciences of the USA, 102, 1626-1631.
66. Parr, L. A., Heintz, M., Lonsdorf, E., & Wroblewski, E. (2010). Visual kin recognition in nonhuman primates (Pan troglodytes and Macaca mulatta): Inbreeding avoidance or male distinctiveness? Journal of Comparative Psychology, 124, 343-350.
67. Penn, D. J. (2002). The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology, 108, 1-21.
68. Penn, D. J., & Potts, W. K. (1999). The evolution of mating preferences and major histocompatibility genes. American Naturalist, 153, 145-164.
69. Piertney, S. B., & Oliver, M. K. (2006). The evolutionary ecology of the major histocompatibility complex. Heredity, 96(1), 7-21.
70. Port, M., & Kappeler, P. M. (2010). The utility of reproductive skew models in the study of male primates: a critical evaluation. Evolutionary Anthropology: Issues, News, and Reviews, 19(2), 46-56.
71. Potts, W. K., & Wakeland, E. K. (1993). Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends in Genetics, 9, 408-412.
72. Rendall, D., Rodman, P. S., & Edmond, R. E. (1996). Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Animal Behaviour, 51, 1007-1015.
73. Robinson, J., Mistry, K., McWilliam, H., Lopez, R., Parham, P., & Marsh, S. G. E. (2011). The IMGT/HLA database. Nucleic Acids Research, 39(Supplement 1), D1171-D1176.
74. Ruff, N. S., Nelson, A. C., Kubinak, J. L., & Potts, W. K. (2012). MHC signaling during social communication. In C. Lopez-Larrea (Ed.), Self and non-self (pp. 290-313). New York: Landes Bioscience and Springer Science+Business Media.
75. Sauermann, U., Nurnberg, P., Bercovitch, F. B., Berard, J. D., Trefilov, A., Widdig, A., Kessler, M., Schmidtke, J., & Krawczak, M. (2001). Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques. Human Genetics, 108(3), 249-254.
76. Schad, J., Sommer, S., & Ganzhorn, J. U. (2004). MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conservation Genetics, 5, 299-309.
77. Schwensow, N., Eberle, M., & Sommer, S. (2008a). Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proceedings of the Royal Society of London B: Biological Sciences, 275(1634), 555-564.
78. Schwensow, N., Fietz, J., Dausmann, K., & Sommer, S. (2008b). MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate. Evolutionary Ecology, 22, 617-636.
79. Sepil, I., Moghadam, H. K., Huchard, E., & Sheldon, B. C. (2012). Characterization and 454 pyrosequencing of major histocompatibility complex class I genes in the great tit reveal complexity in a passerine system. BMC Evolutionary Biology, 12, 68.
80. Setchell, J. M., Charpentier, M. J. E., Abbott, K. M., Wickings, E. J., & Knapp, L. A. (2010). Opposites attract: MHC-associated mate choice in a polygynous primate. Journal of Evolutionary Biology, 23, 136-148.
81. Setchell, J. M., & Huchard, E. (2010). The hidden benefits of sex: evidence for MHC-associated mate choice in primate societies. BioEssays, 32, 940-948.
82. Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to the sex in primates. Advances in the Study of Behaviour, 33, 87-176.
83. Setchell, J. M., Charpentier, M., Abbott, K. A., Wickings, E. J., & Knapp, L. A. (2009). Is brightest best? Testing the Hamilton-Zuk hypothesis in mandrills. International Journal of Primatology, 30, 825-844.
84. Setchell, J. M., Vaglio, S., Abbott, K. M., Moggi-Cecchi, J., Boscaro, F., Pieraccini, G., & Knapp, L. A. (2011). Odour signals major histocompatibility complex genotype in an Old World Monkey. Proceedings of the Royal Society of London B: Biological Sciences, 278, 274-280.
85. Shendure, J., & Ji, H. L. (2008). Next-generation DNA sequencing. Nature Biotechnology, 26, 1135-1145.
86. Sommer, S. (2005). The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology, 2, 16.
87. Sommer, S., Schwab, D., & Ganzhorn, J. U. (2002). MHC diversity of endemic Malagasy rodents in relation to range contraction and social system. Behavioral Ecology and Sociobiology, 51, 214-221.
88. Thom, M. D., Stockley, P., Beynon, R. J., & Hurst, J. L. (2008). Scent, mate choice and genetic heterozygosity. In J. L. Hurst, R. J. Beynon, S. C. Roberts, & T. D. Wyatt (Eds.), Chemical signals in vertebrates 11 (pp. 291-301). New York: Springer.
89. Trivers, R. L. (1972). Parental investment and sexual selection. In P. Campbell (Ed.), Sexual selection and the descent of man (pp. 136-179). London: Heinemann.
90. Tung, J., Alberts, S. C., & Wray, G. A. (2010). Evolutionary genetics in wild primates: combining genetic approaches with field studies of natural populations. Nature Genetics, 26, 353-362.
91. Villinger, J., & Waldman, B. (2012). Social discrimination by quantitative assessment of immunogenetic similarity. Proceedings of the Royal Society of London B: Biological Sciences, 279, 4368-4374.
92. Waldman, B. (1988). The ecology of kin recognition. Annual Review of Ecology and Systematics, 19, 543-571.
93. Wegner, K. M. (2009). Massive parallel MHC genotyping: titanium that shines. Molecular Ecology, 18, 1818-1820.
94. Wegner, K. M., Reusch, T. B. H., & Kalbe, M. (2003). Multiple parasites are driving major histocompatibility complex polymorphism in the wild. Journal of Evolutionary Biology, 16, 224-232.
95. Weisrock, D. W., Rasoloarison, R. M., Fiorentino, I., Ralison, J. M., Goodman, S. M., & Kappeler, P. M. (2010). Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. PloS One, 5, e9883.
96. Widdig, A. (2007). Paternal kin discrimination: the evidence and likely mechanisms. Biological Reviews, 82, 319-334.
97. Willse, A., Kwak, J., Yamazaki, K., Preti, G., Wahl, J. H., & Beauchamp, G. K. (2006). Individual odortypes: interaction of MHC and background genes. Immunogenetics, 58, 967-982.
98. Woelfing, B., Traulsen, A., Milinski, M., & Boehm, T. (2009). Does intra-individual major histocompatibility complex diversity keep a golden mean? Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 117-128.
99. Yamazaki, K., & Beauchamp, G. K. (2007). Genetic basis for MHC-dependent mate choice. Advances in Genetics, 59, 130-145.
100. Yamazaki, K., Beauchamp, G. K., Curran, M., Bard, J., & Boyse, E. A. (2000). Parent-progeny recognition as a function of MHC odortype identity. Proceedings of the National Academy of Sciences of the USA, 97, 10500-10502.
101. Yamazaki, K., Boyse, E. A., Miké, V., Thaler, H. T., Mathieson, B. J., Abbott, J., Boyse, J., Zayas, Z. A., & Thomas, L. (1976). Control of mating preferences in mice by genes in the major histocompatibility complex. The Journal of Experimental Medicine, 144, 1324-1335.
102. Younger, R. M., Amadou, C., Bethel, G., Ehlers, A., Lindahl, K. F., Forbes, S., Horton, R., Milne, S., Mungall, A. J., Trowsdale, J., Volz, A., Ziegler, A., & Beck, S. (2001). Characterization of clustered MHC-linked olfactory receptor genes in human and mouse. Genome Research, 11(4), 519-530.
103. Zagalska-Neubauer, M., Babik, W., Stuglik, M., Guftafsson, L., Cichon, M., & Radwan, J. (2010). 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the collared flycatcher. BMC Evolutionary Biology, 10, 395.