Detective mice assess relatedness in baboons using olfactory cues

Journal of Experimental Biology

Volumn 213, Issue 9, 2010, Pages 1399-1405

  Célérier, Aurélie ^a,b   Huchard, Elise ^a,c,d   Alvergne, Alexandra ^a,c   Féjan, Delphine ^a,c   Plard, Floriane ^b   Cowlishaw, Guy ^e   Raymond, Michel ^a,c   Knapp, Leslie A ^f   Bonadonna, Francesco ^b  

^a UNIV MONTPELLIER   (France)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^d GERMAN PRIMATE CENTER   (Germany)

^e INSTITUTE OF ZOOLOGY   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Baboons; Habituation discrimination task; Kin recognition; Mice; Odour cues; Olfaction

Indexed keywords

ANIMAL; ARTICLE; BABOON; FEMALE; MALE; METABOLISM; MOUSE; ODOR; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PSYCHOLOGICAL ASPECT;

ANIMALS; DISCRIMINATION (PSYCHOLOGY); FEMALE; MALE; MICE; ODORS; PAPIO; SMELL;

ANIMALIA; MAMMALIA; MUS; PAPIO; PAPIO URSINUS; PRIMATES; SIMIIFORMES;

EID: 77951574466     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.038349     Document Type: Article

References (86)

1. Ables, E. M., Kay, L. M. and Mateo, J. M. (2007). Rats asses degree of relatedness from human odors. Physiol. Behav. 90, 726-732.
2. Alvergne, A., Faurie, C. and Raymond, M. (2009). Father-offspring resemblance predicts paternal investment in humans. Anim. Behav. 78, 61-69.
3. Bateson, P. (1983). Mate Choice. Cambridge: Cambridge University Press.
4. Beecher, M. D. (1988). Kin recognition in birds. Behav. Genet. 18, 465-482.
5. Belcher, A. M., Smith, A. B., III, Jurs, P. C., Lavine, B. and Epple, G. (1986). Analysis of chemical signals in a primate species (Saguinus fuscicollis): Use of behavioral, chemical, and pattern recognition methods. J. Chem. Ecol. 12, 513-531.
6. Belcher, A. M., Epple, G., Greenfield, K. L., Richards, L. E., Küderling, I. and Smith, A. B. (1990). Proteins: biologically relevant components of the scent marks of a primate (Saguinus fuscicollis). Chem. Senses 15, 431-446.
7. Bonadonna, F. and Nevitt, G. A. (2004). Partner-specific odor recognition in an Antarctic seabird. Science 306, 835-835
8. Boulet, M., Charpentier, M. J. E. and Drea, C. M. (2009). Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate. BMC Evol. Biol. 9, 281.
9. Breer, H. (2001). Olfaction. In Encyclopedia of Life Sciences (ed. L. C. J. W. Sons), pp. 1-71. London: Nature Publishing Group.
10. Brennan, P. A. and Peele, P. (2003). Towards an understanding of the pregnancyblocking urinary chemosignals of mice. Biochem. Soc. Trans. 31, 152-155.
11. Buchan, J. C., Alberts, S. C., Silk, J. B. and Altmann, J. (2003). True paternal care in a multi-male primate society. Nature 425, 179-181.
12. Busquet, N. and Baudouin, C. (2005). Odour similarities as a basis for discriminating degrees of kinship in rodents: evidence from Mus spicilegus. Anim. Behav. 70, 997-1002. (Pubitemid 41505426)
13. Carroll, L. S., Penn, D. and Potts, W. K. (2002). Discrimination of MHC-derived odors by untrained mice is consistent with divergence in peptide-binding region residues. Proc. Natl. Acad. Sci. USA 99, 2187-2192.
14. Célérier, A., Piérard, C., Rachbauer, D., Sarrieau, A. and Béracochéa, D. (2004). Contextual and serial discriminations: A new learning paradigm to asses simultaneously the effects of acute stress on retrieval of flexible or stable information in mice. Learn. Mem. 11, 196-204.
15. Chapais, B. (2006). Kinship, competence and cooperation in primates. in Cooperation in Primates and Humans: Mechanisms and Evolution (ed. P. M. Kappeler and C. P. van Shaik), pp. 47-64. Berlin, Heidelberg: Springer-Verlag.
16. Charpentier, M. J. E., Boulet, M. and Drea, C. M. (2008). Smelling right: The scent of male lemurs advertises genetic quality and relatedness. Mol. Ecol. 17, 3225-3233.
17. Cheetham, S. A., Thom, M. D., Jury, F., Oilier, W. E. R., Beynon, R. J. and Hurst, J. L. (2007). The genetic basis of individual-recognition signals in the mouse. Curr. Biol. 17, 1771-1777.
18. Clarke, P. M. R., Barrett, L. and Henzi, S. P. (2009). What role do olfactory cues play in chacma baboon mating? Am. J. Primatol. 71, 493-502.
19. Cowlishaw, G. (1999). Ecological and social determinants of spacing behaviour in desert baboon groups. Behav. Ecol. Sociobiol. 45, 67-77.
20. Dasser, V. (1988). A social concept in Java monkeys. Anim. Behav. 36, 225-230.
21. Dominy, N. J. and Lucas, P. W. (2001). Ecological importance of trichromatic vision to primates. Nature 410, 363-366.
22. Drea, C. M., Vignieri, S. N., Kim, H. S., Weldele, M. L. and Glickman, S. E. (2002). Responses to olfactory stimuli in spottedhyenas (Crocuta crocuta): II. discrimination of conspecific scent. J. Comp. Psychol. 116, 342-349.
23. Dugatkin, L. A. (1997). Cooperation Among Animals: An Evolutionary Perspective. Oxford: Oxford University Press.
24. Epple, G. (1986). Communication by chemical signals. In Comparative Primate Biology vol.2A (eds G. Mitchel and J. Erwin), pp. 531-580. New York: Alan R. Liss.
25. Gamboa, G. J., Berven, K. A., Schemidt, R. A., Fishwild, T. G. and Jankens, K. M. (1991). Kin recognition by larval wood frogs (Rana sylvatica): effects of diet and prior exposure to conspecifics. Oecologia 86, 319-324.
26. Gamboa, G. J., Grudzien, T. A., Espelie, K. E. and Bura, E. A. (1996). Kin recognition pheromones in social wasps: combining chemical and behavioural evidence. Anim. Behav. 51, 625-629.
27. Gilad, Y., Wiebe, V., Przeworski, M., Lancet, D. and Pääbo, S. (2004). Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol. 2, 120-125.
28. Gosling, S. D. (2001). From mice to men: what can we learn about personality from animal research? Psychol. Bull. 127, 45-86.
29. Greenberg, L. (1979). Genetic component of bee odor in kin recognition. Science 206, 1095-1097.
30. Halpern, M. and Martínez-Marcos, A. (2003). Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70, 245-318.
31. Halpin, Z. T. (1986). Individual odors among mammals: origins and functions. Adv. Study Behav. 16, 39-70.
32. Hamilton, W. D. (1964). The genetical evolution of social behaviour I & II. J. Theor. Biol. 7, 1-52.
33. Hauber, M. E. and Sherman, P. W. (2001). Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci. 24, 609-616.
34. Hepper, P. G. (1991). Kin Recognition. Cambridge: Cambridge University Press.
35. Heth, G., Todrank, J. and Johnston, R. E. (1998). Kin recognition in golden hamsters: evidence for phenotype matching. Anim. Behav. 56, 409-417. (Pubitemid 28398028)
36. Heymann, E. W. (2006). The neglected sense of smell in primate behavior, ecology and evolution. J. Primatol. 68, 519-524.
37. Holmes, W. G. and Sherman, P. W. (1982). The ontogeny of kin recognition in two species of ground squirrels. Am. Zool. 22, 491-517.
38. Hübener, F. and Laska, M. (1998). Assessing olfactory performance in an Old World primatete, Macaca nemestrina. Physiol. Behav. 64, 521-527.
39. Huchard, E., Alvergne, A., Fejan, D., Knapp, L. A., Cowlishaw, G. and Raymond, M. (2010). More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons, Behav. Ecol. Sociobiol. doi:10.1007/s00265-009-0894-3.
40. Hurst, J. L. and Beynon, R. J. (2004). Scent wars: The chemobiology of competitive signalling in mice. BioEssays 26, 1288-1298.
41. Hurst, J. L., Robertson, D. H. L., Tolladay, U. and Beynon, R. J. (1998). Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55, 1289-1297.
42. Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A. and Beynon, R. J. (2001). Individual recognition in mice mediated by major urinary proteins. Nature 414, 631-634.
43. Jacob, S., McClintock, M. K. and Zelano, B. (2002). Paternally inherited HLA alleles are associated with women's choice of male odor. Wat Genet. 30, 175-179.
44. Kliethermes, C. L. and Crabbe, J. C. (2006). Genetic independence of mouse measures of some aspects of novelty seeking. Proc. Natl. Acad. Sci. USA 103, 5018-5023.
45. Manning, C. J., Wakeland, E. K. and Potts, W. K. (1992). Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360, 581-583. (Pubitemid 23000705)
46. Mardon, J. and Bonadonna, F. (2009). Atypical homing or self-odour avoidance? Blue petrels (Halobaena caerulea) are attracted to their mate's odour but avoid their own Behav. Ecol. Sociobiol. 63, 537-542.
47. Mateo, J. M. (2002). Kin-recognition abilities and nepotism as a function of sociality. Proc. R. Soc. Lond., B, Biol. Sci. 269, 721-727.
48. Mateo, J. M. (2003). Kin recognition in ground squirrels and other rodents. J. Mammal. 84, 1163-1181.
49. Mateo, J. M. (2006a). Development of individually distinct recognition cues. Dev. Psychobiol. 48, 508-519.
50. Mateo, J. M. (2006b). The nature and representation of individual recognition cues in Belding's ground squirrels. Anim. Behav. 71, 141-154.
51. Mateo, J. M. Johnston, R. E. (2003). Kin recognition by self-referent phenotype matching: weighing the evidence. Anim. Cogn. 6, 73-76. (Pubitemid 38260020)
52. Neff, B. D. (2003). Decisions about parental care in response to perceived paternity. Nature 422, 716-719.
53. Neff, B. D. and Sherman, P. W. (2003). Nestling recognition via direct cues by parental male bluegill sunfish (Lepomis macrochirus). Anim. Cogn. 6, 87-92.
54. Neff, B. D. and Sherman, P. W. (2005). In vitro fertilization reveals offspring recognition via self-referencing in a fish with paternal care and cuckoldry. Ethology 111, 425-438.
55. Nevison, C. M., Armstrong, S., Beynon, R. J., Humphries, R. E. and Hurst, J. L. (2003). The ownership signature in mouse scent marks is involatile. Proc. R. Soc. Lond., B, Biol. Sci. 270, 1957-1963.
56. Nevitt, G. A. and Bonadonna, F. (2005). Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol. Lett. 1, 303-305.
57. Novotny, M. V. (2003). Pheromones, binding proteins and receptor responses in rodents. Biochem. Soc. Trans. 31, 117-122.
58. O'Riain, M. J. and Jarvis, J. U. M. (1998). The dynamics of growth in naked molerats: The effects of litter order and changes in social structure. J. Zool. 246, 49-60.
59. Penn, D. and Potts, W. K. (1998). Untrained mice discriminate MHC-determined odors. Physiol. Behav. 63, 235-243.
60. Potts, W. K., Manning, C. J. and Wakeland, E. K. (1991). Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352, 619-621.
61. Reeve, H. K. (1989). The evolution of conspecific acceptance thresholds. Am. Nat. 133, 407.
62. Rendall, D., Rodman, P. S. and Emond, R. E. (1996). Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim. Behav. 51, 1007-1015. (Pubitemid 27003456)
63. Reynolds, J. D. and Sheldon, B. C. (2003). 'Wise fathers'. Nature 422, 669-670.
64. Roser, B., Brown, R. E. and Singh, P. B. (1991). Excretion of transplatation antigens as signals of genetic individuality. New York: Marcel Dekker.
65. Schwagmeyer, P. L. (1988). Scramble-competition polygyny in an asocial mammal: male mobility and mating success. Am. Nat. 131, 885.
66. Scordato, E. S., Dubay, G. and Drea, C. M. (2007). Chemical composition of scent marks in the ringtalled lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures. Chem. Senses 32, 493-504.
67. Setchell, J. M., Vaglio, S., Moggi-Cecchi, J., Boscaro, F., Calamai, L. and Knapp, L. A. (2010). Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): influence of sex, male status, and individual identity. Chem. Senses 35, 205-220.
68. Shepherd, G. M. (2004). The human sense of smell: are we better than we think? PLoS Biol. 2, 572-575.
69. Sherman, P. W., Reeve, H. K. and Pfennig, D. W. (1997). Behavioural Ecology: an Evolutionary Approach. Oxford: Oxford University Press.
70. Singh, P. B., Brown, R. E. and Roser, B. (1987). MHC antigens in urine as olfactory recognition cues. Nature 327, 161.
71. Smith, T. E., Abbott, D. H., Tomlinson, A. J. and Mlotkewicz, J. A. (1997). Differential display of investigative behavior permits discrimination of scent signatures from familiar and unfamiliar socially dominant female marmoset monkeys (Callithrix jacchus). J. Chem. Ecol. 23, 2523-2546.
72. Smith, T. E., Tomlinson, A. J., Mlotkewicz, J. A. and Abbott, D. H. (2001). Female Marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem. Senses 26, 449-458.
73. Smith, K., Alberts, S. C. and Altmann, J. (2003). Wild female baboons bias their social behaviour towards paternal half-sisters. Proc. R. Soc. Lond., B, Biol. Sci. 270, 503-510. (Pubitemid 36308227)
74. Snowdon, C. T., Ziegler, T. E., Schultz-Darken, N. J. and Ferris, C. F. (2006). Social odours, sexual arousal and pairbonding in primates. Philos. Trans. R Soc. Lond., B, Biol. Sci. 361, 2079-2089.
75. Todrank, J., Heth, G. and Johnston, R. E. (1998). Kin recognition in golden hamsters: evidence for kinship odours. Anim. Behav. 55, 377-386. (Pubitemid 28165237)
76. Vokey, J. R. and Rendall, D. (2004). Visual kin recognition and family resemblance in Chimpanzees (Pan troglodytes). J. Comp. Psychol. 118, 194-199.
77. Waldman, B. (1988). The ecology of kin recognition. Annu. Rev. Ecol. Syst. 19, 543-571.
78. Wang, J. (2007). Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet. Res. 89, 135-153.
79. Wedekind, C. and Furi, S. (1997). Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc. R. Soc. Lond., B, Biol. Sci. 264, 1471-1479. (Pubitemid 27480703)
80. Weisfeld, G. E., Czilli, T., Phillips, K. A., Gall, J. A. and Lichtman, C. M. (2003). Possible olfaction-based mechanisms in human in recognition and inbreeding avoidance. J. Exp. Child Psychol. 85, 279-295.
81. Weiss, A., King, J. E. and Perkins, L. (2006). Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelii). J. Pers. Soc. Psychol. 90, 501-511. (Pubitemid 43881473)
82. Widdig, A. (2007). Paternal kin discrimination: The evidence and likely mechanisms. Biol. Rev. 82, 319-334.
83. Wyatt, T. D. (2003). Pheromones and Animal Behaviour, Communication by Smell and Taste. Cambridge: Cambridge University Press.
84. Yamazaki, K., Yamaguchi, M., Baranoski, L., Bard, J., Boyse, E. A. and Thomas, L. (1979). Recognition among mice. Evidence from the use of a Y-maze differentially scented by congenie mice of different major histocompatibility types. J. Exp. Med. 150, 755-760. (Pubitemid 10227327)
85. Yamazaki, K., Beauchamp, G. K., Egorov, I. K., Bard, J., Thomas, L. and Boyse, E. A. (1983). Sensory distinction between H-2b and H-2bml mutant mice. Proc. Natl. Acad. Sci. USA 80, 5685-5688.
86. Zhang, J. X., Soini, H. A., Bruce, K. E., Wiesler, D., Woodley, S. K., Baum, M. J. and Novotny, M. V. (2005). Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem. Senses 30, 727-737. (Pubitemid 41672214)