Olfactory signals and the MHC: A review and a case study in Lemur catta

American Journal of Primatology

Volumn 68, Issue 6, 2006, Pages 568-584

  Knapp, Leslie A ^a   Robson, Julie ^a   Waterhouse, John S ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

Author keywords

Lemur catta; Major histocompatibility complex (MHC); Olfaction

Indexed keywords

DISEASE RESISTANCE; GAS CHROMATOGRAPHY; GENE EXPRESSION; GENETIC ANALYSIS; GENOTYPE; IMMUNE RESPONSE; KIN SELECTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MAMMAL; MASS SPECTROMETRY; MATE CHOICE; REPRODUCTIVE BEHAVIOR; SOCIAL BEHAVIOR; VOLATILE SUBSTANCE;

ALLELE; ANIMAL; ANIMAL COMMUNICATION; CONFERENCE PAPER; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MASS FRAGMENTOGRAPHY; METABOLISM; ODOR; PHYSIOLOGY; PROSIMIAN; RODENT; SIGNAL TRANSDUCTION;

ALLELES; ANIMAL COMMUNICATION; ANIMALS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENOTYPE; HUMANS; LEMUR; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; ODORS; POLYMORPHISM, GENETIC; RODENTIA; SIGNAL TRANSDUCTION; SMELL;

ANIMALIA; LEMUR CATTA; LEMURIDAE; PRIMATES; RODENTIA; VERTEBRATA;

EID: 33745574053     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20253     Document Type: Conference Paper

References (68)

1. Barrett J, Abbott DH, George LM. 1990. Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. J Reprod Fertil 90:411-418.
2. Beauchamp GK, Yamazaki K. 2001. Chemical signalling in mice. Biochem Soc Trans 31:147-151.
3. Beck S, Trowsdale J. 2000. The human major histocompatability complex: lessons from the DNA sequence. Annu Rev Genomics Hum Genet 1:117-137.
4. Belcher A, Epple G, Kuderling I, Smith AB. 1988. Volatile components of scent material from cotton-top tamarin (Saguinus O. oedipus). J Chem Ecol 14:1367-1384.
5. Bontrop RE, Otting N, de Groot NG, Doxiadis GG. 1999. Major histocompatibility complex class II polymorphisms in primates. Immunol Rev 167:339-350.
6. Brown RE, Singh PB, Roser B. 1987. The major histocompatibility complex and the chemosensory recognition of individuality in rats. Physiol Behav 40:65-73.
7. Buesching CD, Waterhouse JS, Macdonald DW. 2002a. Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) part I: chemical differences related to individual parameters. J Chem Ecol 28:41-56.
8. Buesching CD, Waterhouse JS, Macdonald DW. 2002b. Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) part II: time-related variation in the individual-specific composition. J Chem Ecol 28:57-69.
9. Cernoch JM, Porter RH. 1985. Recognition of maternal axillary odors by infants. Child Dev 56:1593-1598.
10. Eggert F, Muller-Ruchholtz W, Ferstl R. 1999. Olfactory cues associated with the major histocompatibility complex. Genetica 104:191-197.
11. Egid K, Brown JL. 1989. The major histocompatibility complex and female mating preferences in mice. Anim Behav 38:548-550.
12. Epple G, Katz Y. 1984. Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis). Am J Primatol 6:215-227.
13. Epple G. 1986. Communication by chemical signals. In: Mitchell G, Erwin J, editors. Comparative primate biology, vol 2A: behavior, conservation, and ecology. New York: Alan R. Liss. p 531-580.
14. Ferstl R, Eggert F, Westphal E, Zavazava N, Muller-Ruchholtz W. 1992. MHC-related odors in humans. In: Doty RL, Muller-Schwarze D, editors. Chemical signals in vertebrates. New York: Plenum Press. p 206-211.
15. Gilbert AN, Yamazaki K, Beauchamp GK, Thomas L. 1986. Olfactory discrimination of mouse strains (Mus musculus) and major histocompatibility types by humans (Homo sapiens). J Comp Psychol 100:262-265.
16. 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.
17. Gorman ML. 1976. A mechanism for individual recognition by odour in Herpestes auropunctatus. Anim Behav 24:141-146.
18. Hayes RA, Morelli T-L, Wright PC. 2004. Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli: a preliminary chemical examination. Am J Primatol 63:49-62.
19. Hayes RA, Morelli T-L, Wright P. 2005. The chemistry of scent marking in two lemurs: Lemur catta and Propithecus verreauxi coquereli. In: Mason RT, Le Master MP, Müller-Schwarze D, editors. Chemical signals in vertebrates X. New York: Kluwer. p 159-167.
20. Hedrick PW, Black FL. 1997. HLA and mate selection: no evidence in South Amerindians. Am J Hum Genet 61:505-511.
21. Heymann E. 2004. The neglected sense-olfaction in primate behaviour, ecology and evolution. Folia Primatol 75:45.
22. Holmes WG, Sherman PW. 1982. The ontogeny of kin recognition in two species of ground-squirrels. Am Zool 22:491-517.
23. Hughes AL, Hughes MK. 1995. Natural selection on the peptide-binding regions of major histocompatibility complex molecules. Immunogenetics 42:233-243.
24. Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE, Robertson DH, Cavaggioni A, Beynon RJ. 2001. Individual recognition in mice mediated by major urinary proteins. Nature 414:631-634.
25. Jacob S, McClintock MK, Zelano B, Ober C. 2002. Paternally inherited HLA alleles are associated with women's choice of male odor. Nat Genet 30:175-179.
26. Jolly A. 1966. Lemur behavior: a Madagascar field study. Chicago: University of Chicago Press.
27. Kavaliers M, Colwell DD. 1995. Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond B Biol Sci 261:31-35.
28. Klein J. 1986. Natural history of the major histocompatibility complex. New York: Wiley.
29. Knapp LA, Cadavid LF, Eberle ME, Knechtle SJ, Bontrop RE, Watkins DI. 1997a. Identification of new Mamu-DRB alleles using DGGE and direct sequencing. Immunogenet 45:171-179.
30. Knapp LA, Lehmann E, Hennes L, Eberle ME, Watkins DI. 1997b. High-resolution HLA-DRB typing using DGGE and direct sequencing. Tissue Antigens 50:170-177.
31. Knapp LA. 2005. The ABCs of MHC. Evol Anthropol 14:28-37.
32. Kruuk H, Gorman ML, Leitch A. 1984. Scent-marking with the subcaudal gland by the European badger, Meles meles. Anim Behav 32:899-907.
33. Leinders-Zufall T, Brennan P, Widmayer P, Chandramani SP, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T. 2004. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033-1037.
34. Manning CJ, Wakeland EK, Potts WK. 1992. Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360:581-583.
35. Mateo JM, Johnston RE. 2000. Kin recognition and the "armpit effect": evidence of self-referent phenotype matching. Proc R Soc Lond B Biol Sci 267:695-700.
36. McClintock MK. 1983. Modulation of the estrous-cycle by pheromones from pregnant and lactating rats. Biol Reprod 28:823-829.
37. McClintock MK. 2000. Human pheromones: primers, releasers, signalers, or modulators? In: Wallen K, Schneider JE, editors. Reproduction in context. Cambridge, MA: MIT. p 355-420.
38. Mertl AS. 1975. Discrimination of individuals by scent in primates. Behav Biol 14:505-509.
39. Middleton SA, Anzenberger G, Knapp LA. 2004. Identification of MHC-DRB alleles in New World monkeys using PCR, DGGE and direct sequencing. Immunogenetics 55:785-790.
40. 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.
41. Pearse-Pratt R, Schellinck H, Brown R, Singh PB, Roser B. 1999. Soluble MHC antigens and olfactory recognition of genetic individuality: the mechanism. Genetica 104:223-230.
42. Penn D, Potts WK. 1998a. Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391-396.
43. Penn D, Potts WK. 1998b. Untrained mice discriminate MHC-determined odors. Physiol Behav 64:235-243.
44. Penn DJ, Potts WK. 1999. The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145-164.
45. Penn DJ. 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1-21.
46. Perret M. 1995. Chemocommunication in the reproductive function of mouse lemurs. In: Alterman L, Doyle GA, Izard MK, editors. Creatures of the dark: the nocturnal prosimians. New York: Plenum Press. p 377-391.
47. Porter RH, Tepper VJ, White DM. 1981. Experiential influences on the development of huddling preferences and sibling recognition in spiny mice. Dev Psychobiol 14:375-382.
48. Porter RH, Cernoch JM, McLaughlin FJ. 1983. Maternal recognition of neonates through olfactory cues. Physiol Behav 30:151-154.
49. Porter RH, Cernoch JM, Balogh RD. 1985. Odor signatures and kin recognition. Physiol Behav 34:445-448.
50. Potts WK, Manning CJ, Wakeland EK. 1991. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352:619-621.
51. Rasmussen LEL. 1999. Chemical communication: an integral part of functional Asian elephant (Elephas maximus) society. J Biosci 24:241-251.
52. Rasmussen LEL, Riddle HS, Krishnamurthy V. 2002. Mellifluous matures to malodorous in musth. Nature 415:975-976.
53. Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SG. 2003. IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31:311-314.
54. Schilling A. 1979. Olfactory communication in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press.
55. Schulte BA, Rasmussen LEL. 1999. Musth, sexual selection, testosterone, and metabolites. In: Johnston RE, Müller-Schwarze D, Sorensen PW, editors. Advances in chemical signals in vertebrates. New York: Kluwer Academic Publishers. p 383-398.
56. Smith TE, Tomlinson AJ, Mlotkiewicz JA, Abbott DH. 2001. Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem Senses 26:449-458.
57. Sun LX, Muller-Schwarze D. 1997. Sibling recognition in the beaver: a field test for phenotype matching. Anim Behav 54:493-502.
58. Thomas L. 1975. Symbiosis as an immunological problem. In: Neter E, Milgrom F, editors. Fourth International Congress of Immunology. New York: Karger. p 2-11.
59. 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.
60. Wedekind C, Furi S. 1997. Body odour preferences in men and women: do they aim for specific combinations or simple heterozygosity? Proc R Soc Lond B Biol Sci 264:1471-1479.
61. Willis CM, Church SM, Guest CM, Cook WA, McCarthy N, Bransbury AJ, Church MR, Church JC. 2004. Olfactory detection of human bladder cancer by dogs: proof of principle study. BMJ 329:712.
62. Wyatt TD. 2003. Pheromones and animal behaviour. Cambridge: Cambridge University Press.
63. Yamazaki K, Yamaguchi M, Andrews PB, Peake B, Boyse EA. 1978. Mating preferences of F2 segregants of crosses between MHC-congenic mouse strains. J Immunogenet 6:253-259.
64. Yamazaki K, Yamaguchi M, Baranoski L, Bard J, Boyse EA, Thomas L. 1979. Recognition among mice. Evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatibility types. J Exp Med 150:755-760.
65. Yamazaki K, Beauchamp GK, Egorov IK, Bard J, Thomas L, Boyse EA. 1983. Sensory distinction between H-2b and H-2bm1 mutant mice. Proc Natl Acad Sci USA 80:5685-5688.
66. Yamazaki K, Beauchamp GK, Shen FW, Bard J, Boyse EA. 1991. A distinctive change in odor type determined by H-2D/L mutation. Immunogenetics 34:129-131.
67. Yamazaki K, Beauchamp GK, Curran M, Bard J, Boyse EA. 2000. Parent-progeny recognition as a function of MHC odortype identity. Proc Natl Acad Sci USA 97:10500-10502.
68. Yarger RG, Smith AB, Preti G, Epple G. 1977. The major volatile constituents of the scent mark of a South American primate, Saguinus fuscicollis. Callitrichidae. J Chem Ecol 3:45-56.