Nasopalatine ducts and flehmen behavior in the mandrill: Reevaluating olfactory communication in old world primates

American Journal of Primatology

Volumn 75, Issue 7, 2013, Pages 703-714

  Charpentier, Marie J E ^a   Mboumba, Sylvère ^b   Ditsoga, Claude ^b   Drea, Christine M ^c  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

^c DUKE UNIVERSITY   (United States)

Author keywords

Behavioral bioassay; Catarrhine; Chemosignal; Flehmen; Incisive duct; Pheromone

Indexed keywords

ANATOMY; BEHAVIORAL ECOLOGY; BIOASSAY; BIOLOGICAL UPTAKE; BREEDING SEASON; CHEMICAL CUE; COMMUNICATION BEHAVIOR; GENETIC ANALYSIS; MORPHOLOGY; ODOR; OLFACTORY CUE; PHYSIOLOGICAL RESPONSE; PRIMATE; SIGNALING; VOLATILE SUBSTANCE;

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; FEMALE; MALE; MANDRILLUS; ODOR; PHYSIOLOGY;

ANIMAL COMMUNICATION; ANIMALS; FEMALE; MALE; MANDRILLUS; SMELL;

MAMMALIA; MANDRILLUS; MANDRILLUS SPHINX; PRIMATES;

EID: 84877924569     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22146     Document Type: Article

References (118)

1. Adipietro KA, Mainland JD, Matsunami H. 2012. Functional evolution of mammalian odorant receptors. PLoS Genet 8:e1002821.
2. Ankel-Simons F. 2000. Primate anatomy: an introduction. New York: Academic Press. p 506.
3. Aujard F. 1997. Effect of vomeronasal organ removal on male socio-sexual responses to female in a prosimian primate (Microcebus murinus). Physiol Behav 62:1003-1008.
4. Baenninger R. 1987. Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J Comp Psychol 101:349-354.
5. Bailey K. 1978. Flehmen in the ring-tailed lemur (Lemur catta). Behaviour 65:309-319.
6. Barton RA. 1998. Visual specialization and brain evolution in primates. Proc R Soc B Biol Sci 265:1933-1937.
7. Barton RA. 2006. Olfactory evolution and behavioral ecology in primates. Am J Primatol 68:545-558.
8. Berghard A, Buck LB, Liman ER. 1996. Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc Natl Acad Sci USA 93:2365-2369.
9. Bhatnagar KP, Smith TD. 2001. The human vomeronasal organ: III. Postnatal development from infancy through the ninth decade. J Anat 199:289-302.
10. Boehm N, Gasser B. 1993. Sensory receptor-like cells in the human foetal vomeronasal organ. Neuroreport 4:867-870.
11. Boehm N, Roos J, Gasser B. 1994. Luteinizing hormone releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses. Dev Brain Res 82:175-180.
12. Boehm U, Zou ZH, Buck LB. 2005. Feedback loops link odor and pheromone signaling with reproduction. Cell 123:683-695.
13. Borcherding F, Wöhrmann-Repenning A. 2007. Taste buds and vomeronasal olfaction in some primates. Mamm Biol 72:174-178.
14. Charpentier M, Peignot P, Hossaert-McKey M, et al. 2005. Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behav Ecol 16:614-623.
15. Charpentier MJE, Crawford JC, Boulet M, Drea CM. 2010. Message 'scent': lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Anim Behav 80:101-108.
16. Crawford J, Boulet M, Drea CM. 2011. Smelling wrong: hormonal contraception in lemurs alters critical female odour cues. Proc R Soc B Biol Sci 278:122-130.
17. Crowell-Davis S, Houpt KA. 1985. The ontogeny of flehmen in horses. Animl Behav 33:739-745.
18. Curtis RF, Ballantine JA, Keverne EB, Bonsall RW, Michael RP. 1971. Identification of primate sexual pheromones and the properties of synthetic attractants. Nature 233:396-398.
19. Darwin C. 1871. The descent of man, and selection in relation to sex. Reprinted in 1998. London: John Murray. p 791.
20. de Jong YA, Butynski TM. 2010. Three Sykes's monkey Cercopithecus mitis×vervet monkey Chlorocebus pygerythrus hybrids in Kenya. Primate Conserv 25:43-56.
21. Del Punta K, Leinders-Zufall T, Rodriguez I, et al. 2002. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70-74.
22. Dixson AF. 1998. Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press. p 546.
23. Dixson AF, Bossi T, Wickings EJ. 1993. Male dominance and genetically determined reproductive success in the mandrill (Mandrillus sphinx). Primates 34:525-532.
24. Doving KB, Trotier D. 1998. Structure and function of the vomeronasal organ. J Exp Biol 201:2913-2925.
25. Drea CM, Scordato ES. 2007. Olfactory communication in the ringtailed lemur (Lemur catta): form and function of multimodal signals. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt T, editors. Chemical signals in vertebrates II. New York: Springer Press. p 91-102.
26. Dugmore SJ, Bailey K, Evans CS. 1984. Discrimination by male ring-tailed lemurs (Lemur catta) between the scent marks of male and those of female conspecifics. Int J Primatol 5:235-245.
27. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
28. Dulac C, Torello AT. 2003. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551-562.
29. Dulac C, Wagner S. 2006. Genetic analysis of brain circuits underlying pheromone signaling. Ann Rev Genet 40:449-467.
30. Epple G. 1974. Primate pheromones. In: Birch MC, editor. Pheromones. Amsterdam: North Holland Publishing Co. p 366-385.
31. Epple G, Belcher AM, Küderling I, et al. 1993. Making sense out of scents: species differences in scent glands, scent-marking behaviour, and scent-mark composition in the Callitrichidae. In: Rylands AB, editor. Marmosets and Tamarins: systematics, behaviour, and ecology. Oxford: Oxford University Press. p 123-151.
32. Estes RD. 1972. The role of the vomeronasal organ in mammalian reproduction. Mammalia 36:315-341.
33. Evans CS. 2006. Accessory chemosignaling mechanisms in primates. Am J Primatol 68:525-544.
34. Evans CS, Schilling A. 1995. The accessory (vomeronasal) chemoreceptor system in some prosimians. In: Alterman L, Doyle GA, Izard MK, editors. Creatures of the dark: The nocturnal prosimians. New York: Plenum Press. p 393-411.
35. Feistner ATC. 1991. Scent marking in mandrills, Mandrillus sphinx. Folia Primatol 57:42-47.
36. Freeman NJ, Pasternak GM, Rubi TL, Barrett L, Henzi SP. 2012. Evidence for scent marking in vervet monkeys? Primates 53:311-315.
37. Frets GP. 1914. Beiträge zur vergleichenden Anatomie und Embryologie der Nase der Primaten. Gegenbaurs Morphol Jahrb 48:239-279.
38. Geissman T. 1987. A sternal gland in the siamang gibbon (Hylobates syndactylus). Int J Primatol 8:1-16.
39. Giorgi D, Rouquier S. 2002. Identification of V1R-like putative pheromone receptor sequences in non-human primates. Characterization of V1R pseudogenes in marmoset, a primate species that possesses an intact vomeronasal organ. Chem Senses 27:529-537.
40. Halpern M. 1987. The organization and function of the vomeronasal system. Ann Rev Neurosci 10:325-362.
41. Halpern M, Martínez-Marcos A. 2003. Structure and function of the vomeronasal system: an update. Progr Neurobiol 70:245-318.
42. Hart BL, Hart LA, Maina JN. 1988. Alteration in vomeronasal system anatomy in alcelaphine antelopes: correlation with alteration in chemosensory investigation. Physiol Behav 42:155-162.
43. Hart BL, Leedy MG. 1987. Stimulus and hormonal determinants of flehmen behavior in cats. Horm Behav 21:44-52.
44. Hendrickx A. 1971. Embryology of the baboon. Chicago: University of Chicago Press.
45. Heymann EW. 2006. The neglected sense-olfaction in primate behavior, ecology, and evolution. Am J Primatol 68:519-524.
46. Hill WCO. 1970. Primates: comparative anatomy and taxonomy, VIII-Cynopithecinae (Papio, Mandrillus, Theropithecus). Edinburgh: Edinburgh University Press. p. 680.
47. Hill WCO. 1974. Primates: comparative anatomy and taxonomy, VII-Cynopithecinae (Cercocebus, Macaca, Cynopithecis). Edinburgh: Edinburgh University Press.
48. Hofer HO. 1977. The anatomical relations of the ductus vomeronasalis and the occurrence of taste buds in the papilla palatine of Nycticebus coucang (Primates, Prosimiae) with remarks on Strepsirrhinism. Gegenbaurs Morphol Jahrb 123:836-856.
49. Hübener F, Laska M. 1998. Assessing olfactory performance in an Old World primate, Macaca nemestrina. Physiol Behav 64:521-527.
50. Hunter AJ, Fleming D, Dixson AF. 1984. The structure of the vomeronasal organ and nasopalatine ducts in Aotus trivirgatus and some other primate species. J Anat 138:217-225.
51. 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.
52. Johnson A, Josephson R, Hawke M. 1985. Clinical and histological evidence for the presence of the vomeronasal (Jacobson's) organ in adult humans. J Otolaryngol 14:71-79.
53. Johnston RE. 1998. Pheromones, the vomeronasal system, and communication: from hormonal responses to individual recognition. Ann N Y Acad Sci 104:34-40.
54. Jolly A. 1966. Lemur behavior: a Madagascar field study. Chicago: The University of Chicago Press.
55. Jordan J. 1972. The vomeronasal organ (of Jacobson) in primates. Folia Morphol 31:418-432.
56. Keller M, Baumb MJ, Brock O, Brennand PA, Bakker J. 2009. The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav Brain Res 200:268-276.
57. Kimchi T, Xu J, Dulac C. 2007. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009-1014.
58. Kouros-Mehr H, Pintchovski S, Melnyk J, et al. 2001. Identification of non-functional human VNO receptor genes provides evidence for vestigiality of the human VNO. Chem Senses 26:1167-1174.
59. Ladewig J, Hart BL. 1980. Flehmen and vomeronasal organ function in male goats. Physiol Behav 24:1067-1071.
60. Laska M, Wieser A, Salazar LTH. 2005. Olfactory responsiveness to two odorous steroids in three species of nonhuman primates. Chem Senses 30:505-511.
61. Leonhardt SD, Tung J, Camden JB, Leal M, Drea M. 2009. Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. Behav Ecol 20:1-12.
62. Leypold BG, Yu CR, Leinders-Zufall T, et al. 2002. Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci USA 99:6376-6381.
63. Liberles SD. 2009. Trace amine-associated receptors are olfactory receptors in vertebrates. Ann N Y Acad Sci 1170:168-172.
64. Liberles SD, Buck LB. 2006. A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645-650.
65. Liman ER, Corey DP, Dulac C. 1999. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci USA 96:5791-5796.
66. Liman ER, Innan H. 2003. Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100:3328-3332.
67. Lin DY, Zhang SZ, Block E, Katz LC. 2005. Encoding social signals in the mouse main olfactory bulb. Nature 434:470-477.
68. Lindsay FEF, Burton FL. 1983. Observational study of "urine testing" in the horse and donkey stallion. Equine Vet J 15:330-336.
69. Loireau J-N, Gautier-Hion A. 1988. Olfactory marking behaviour in guenons and its implications. In: Gautier-Hion A, Bourlière F, Gautier J-P, Kingdon J, editors. A primate radiation: evolutionary biology of the African guenons. Cambridge: Cambridge University Press. p 247-253.
70. Loo S. 1973. A comparative study of the nasal fossa of four nonhuman primates. Folia Primatol 20:410-422.
71. Maier W. 1997. The nasopalatine duct and the nasal floor cartilages in catarrhine primates. Zeitschrift fuer Morphologie und Anthropologie 81:289-300.
72. Matsui A, Go Y, Niimura Y. 2010. Degeneration of olfactory receptor gene repertories in primates: no direct link to full trichromatic vision. Mol Biol Evol 27:1192-1200.
73. Melese-d'Hospital PY, Hart BL. 1985. Vomeronasal organ cannulation in male goats-evidence for transport of fluid from oral cavity to vomeronasal organ during flehmen. Physiol Behav 35:941-944.
74. Mendoza AS, Künderling I, Kuhn HJ, Kühnel W. 1994. The vomeronasal organ of the New World monkey Saguinus fuscicollis (Callitrichidae). A light and transmission electron microscopic study. Ann Anat 176:217-222.
75. Meredith M. 1994. Chronic recording of vomeronasal pump activation in awake behaving hamsters. Physiol Behav 56:345-354.
76. Meredith M. 2001. Human vomeronasal organ function: a critical review of best and worst cases. Chem Senses 26:433-445.
77. Meredith M, Marques DM, O'Connell RO, Stern FL. 1980. Vomeronasal pump: significance for male hamster sexual behavior. Science 207:1224-1226.
78. Michael RP, Keverne EB. 1968. Pheromones in the communication of sexual status in primates. Nature 218:746-749.
79. Milinski M, Wedekind C. 2001. Evidence for MHC-correlated perfume preferences in humans. Behav Ecol 12:140-149.
80. Müller-Schwarze D. 2006. Chemical ecology of vertebrates. Cambridge: Cambridge University Press. p. 578.
81. Ober C. 1999. Studies of HLA, fertility and mate choice in a human isolate. Hum Reprod Update 5:103-107.
82. Pantages E, Dulac C. 2000. A novel family of candidate pheromone receptors in mammals. Neuron 28:835-845.
83. Penn DJ, Oberzaucher E, Grammer K, et al. 2007. Individual and gender fingerprints in human body odour. J R Soc Interface 4:331-340.
84. Rasmussen LEL. 1998. Chemical communication: an integral part of functional Asian elephant (Elephas maximus) society. Ecoscience 5:411-429.
85. Renoult JP, Schaefer HM, Sallé B, Charpentier MJE. 2011. The evolution of the multicoloured face of mandrills: insights from the perceptual space of colour vision. PLoS ONE 6:e29117.
86. Salazar I, Quinteiro PS, Cifuentes JM. 1997. The soft-tissue components of the vomeronasal organ in pigs, cows and horses. Anat Histol Embryol 26:179-186.
87. Sankar R, Archunan G. 2002. Occurrence of flehmen reaction in bull towards bovine (Bos taurus) oestrus urine. J Endocrinol Reprod 6:61.
88. Schaal B, Doucet S, Sagot P, Hertling E, Soussignan R. 2006. Human breast areolae as scent organs: morphological data and possible involvement in maternal-neonatal coadaptation. Dev Psychobiol 48:100-110.
89. Schaal B, Durand K. 2012. The role of olfaction in human multisensory development. In: Bremner AJ, Lewkowicz DJ, Spence C, editors. Multisensory development. Oxford: Oxford University Press. p 29-61.
90. Schilling A. 1979. Olfactory communication in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 461-542.
91. Schilling A, Serviere J, Gendrot G, Perret M. 1990. Vomeronasal activation by urine in the primate Microcebus murinus: a 2 DG study. Exp Brain Res 81:609-618.
92. Schmidt M, Wöhrmann-Repenning A. 2004. Suggestions for the functional relationship between differently located taste buds and vomeronasal olfaction in several mammals. Mamm Biol 69:311-318.
93. Schneider KM. 1930. Drawing back of the upper lip. Der Zoologische Garten 3:183-198.
94. Scordato ES, Drea CM. 2007. Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim Behav 73:301-314.
95. Setchell JM. 1999. Socio-sexual development in the male mandrill (Mandrillus sphinx). Cambridge (UK): University of Cambridge.
96. Setchell JM, Dixson AF. 2001. Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx). Am J Primatol 53:109-121.
97. Setchell JM, Vaglio S, Abbott KM, et al. 2011. Odour signals major histocompatibility complex genotype in an Old World monkey. Proc R Soc B 278:274-280.
98. Setchell JM, Vaglio S, Moggi-Cecchi J, et al. 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.
99. Setchell JM, Wickings EJ. 2004. Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx). Am J Phys Anthropol 125:73-84.
100. Setchell JM, Wickings EJ. 2005. Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25-50.
101. Setchell JM, Wickings EJ, Knapp LA. 2006. Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association. Am J Phys Anthropol 131:498-510.
102. Smith TD, Bhatnagar KP, Shimp KL, et al. 2002. Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates. Anat Rec (New Anat) 267:166-176.
103. Smith TD, Garrett EC, Bhatnagar KP, et al. 2011. The vomeronasal organ of New World primates (Platyrrhini). Anat Rec 294:2158-2178.
104. Smith TD, Siegel MI, Bhatnagar KP. 2001a. Reappraisal of the vomeronasal system of catarrhine primates: ontogeny, morphology, functionality, and persisting questions. Anat Rec (New Anat) 265:176-192.
105. Smith TD, Siegel MI, Bonar CJ, et al. 2001b. The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology to that of humans. J Anat 198:77-82.
106. Smith TD, Siegel MI, Burrows AM, et al. 1998. Searching for the vomeronasal organ of adult humans: preliminary findings on location, structure, and size. Microsc Res Tech 41:483-491.
107. Stowers L, Holy TE, Meister M, Dulac C, Koentges G. 2002. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493-1500.
108. Trotier D, Eloit C, Wassef M, et al. 2000. The vomeronasal cavity in adult humans. Chem Senses 25:369-380.
109. Wedekind C, Furi S. 1997. Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc R Soc Lond Series B Biol Sci 264:1471-1479.
110. Wickings EJ. 1995. Genetic self-management in a captive colony of mandrills (Mandrillus sphinx) as revealed by DNA minisatellite fingerprints. Electrophoresis 16:1678-1683.
111. Wilson D, Hendrickx A. 1977. Quantitative aspects of proliferation in the nasal epithelium of the rhesus monkey embryo. Embryol Exp Morphol 38:217-226.
112. Wöhrmann-Repenning A. 1978. Taste bud on the papilla palatina of Tupaia glis (Diard 1820), its occurrence and relationship to Jacobson's organ. Gegenbaurs Morphol Jahrb 124:375-384.
113. Wolowich CK, Evans S. 2007. Sociosexual behavior and chemical communication of Aotus nancymaae. Int J Primatol 28:1299-1313.
114. Won J, Mair EA, Bolger WE, Conran RM. 2000. The vomeronasal organ: an objective anatomic analysis of its prevalence. Ear Nose Throat J 79:600-605.
115. Xu F, Schaefer M, Kida I, et al. 2005. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Compar Neurol 489:491-500.
116. Yoon HY, Enquist LW, Dulac C. 2005. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123:669-682.
117. Zhang JZ, Webb DM. 2003. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100:8337-8341.
118. Zingeser MR. 1984. The nasopalatine ducts and associated structures in the Rhesus monkey (Macaca mulatta): topography, prenatal development, function, and phylogeny. Am J Anat 170:581-595.