The evolution of pheromonal communication

Behavioural Brain Research

Volumn 200, Issue 2, 2009, Pages 239-247

  Swaney, William T ^a   Keverne, Eric B ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amphibians; Evolution; Mammals; Olfaction; Pheromone; Primates; Vomeronasal

Indexed keywords

PHEROMONE;

AMPHIBIA; ARTICLE; BRAIN SIZE; DEVONIAN; GENE INACTIVATION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; RODENT; SENSORY SYSTEM; SOCIAL BEHAVIOR; VOMERONASAL ORGAN;

AMPHIBIANS; ANIMAL COMMUNICATION; ANIMALS; BRAIN; EVOLUTION; GENETIC VARIATION; HUMANS; MAMMALS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PHEROMONES; PHEROMONES, HUMAN; SMELL; VOMERONASAL ORGAN;

EID: 64049093013     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.09.039     Document Type: Article

References (91)

1. Aujard F., Schilling A., and Perret M. Gonadotropin-releasing hormone (GnRH) immunoreactive neurons in male mouse lemurs following removal of the vomeronasal organ. Brain Res 1043 (2005) 247-250
2. Barrett J., Abbott D.H., and George L.M. Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. J Reprod Fertil 90 (1990) 411-418
3. Barrett J., Abbott D.H., and George L.M. Sensory cues and the suppression of reproduction in subordinate female marmoset monkeys, Callithrix jacchus. J Reprod Fertil 97 (1993) 301-310
4. Barton R.A., Purvis A., and Harvey P.H. Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos Trans R Soc Lond B: Biol Sci 348 (1995) 381-392
5. Barton R.A. Olfactory evolution and behavioral ecology in primates. Am J Primatol 68 (2006) 545-558
6. Baxi K.N., Dorries K.M., and Eisthen H.L. Is the vomeronasal system really specialized for detecting pheromones?. Trends Neurosci 29 (2006) 1-7
7. Bertmar G. Evolution of vomeronasal organs in vertebrates. Evolution 35 (1981) 359-366
8. Beynon R.J., and Hurst J.L. Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31 (2003) 142-146
9. Brechbuhl J., Klaey M., and Broillet M.C. Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science 321 (2008) 1092-1095
10. Brennan P.A., Schellinck H.M., and Keverne E.B. Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience 90 (1999) 1463-1470
11. Brennan P.A., and Kendrick K.M. Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B: Biol Sci 361 (2006) 2061-2078
12. Bruce H.M. An exteroceptive block to pregnancy in the mouse. Nature 184 (1959) 105
13. Buck L., and Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65 (1991) 175-187
14. Buck L.B. The molecular architecture of odor and pheromone sensing in mammals. Cell 100 (2000) 611-618
15. Curley J.P., and Keverne E.B. Genes, brains and mammalian social bonds. Trends Ecol Evol 20 (2005) 561-567
16. Date-Ito A., Ohara H., Ichikawa M., Mori Y., and Hagino-Yamagishi K. Xenopus V1R vomeronasal receptor family is expressed in the main olfactory system. Chem Senses 33 (2008) 339-346
17. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., et al. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419 (2002) 70-74
18. Dorries K.M., Adkins-Regan E., and Halpern B.P. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol Behav 57 (1995) 255-259
19. Dorries K.M., Adkins-Regan E., and Halpern B.P. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol 49 (1997) 53-62
20. Doving K.B., and Trotier D. Structure and function of the vomeronasal organ. J Exp Biol 201 (1998) 2913-2925
21. Dulac C., and Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83 (1995) 195-206
22. Dunbar R.I.M., and Shultz S. Evolution in the social brain. Science 317 (2007) 1344-1347
23. Eisthen H.L. Evolution of vertebrate olfactory systems. Brain Behav Evol 50 (1997) 222-233
24. Eisthen H.L. The goldfish knows: olfactory receptor cell morphology predicts receptor gene expression. J Comp Neurol 477 (2004) 341-346
25. Eisthen H.L. Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Microsc Res Tech 23 (1992) 1-21
26. Eisthen H.L. Presence of the vomeronasal system in aquatic salamanders. Philos Trans R Soc Lond B: Biol Sci 355 (2000) 1209-1213
27. Elsaesser R., Montani G., Tirindelli R., and Paysan J. Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium. Eur J Neurosci 21 (2005) 2692-2700
28. Fernandez-Fewell G.D., and Meredith M. c-Fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance. J Neurosci 14 (1994) 3643-3654
29. Firestein S. How the olfactory system makes sense of scents. Nature 413 (2001) 211-218
30. Gilad Y., Bustamante C.D., Lancet D., and Paabo S. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am J Hum Genet 73 (2003) 489-501
31. Gilad Y., Man O., Paabo S., and Lancet D. Human specific loss of olfactory receptor genes. Proc Natl Acad Sci USA 100 (2003) 3324-3327
32. Gilad Y., Przeworski M., and Lancet D. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2 (2004) E5
33. Grus W.E., Shi P., Zhang Y.P., and Zhang J. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 102 (2005) 5767-5772
34. Grus W.E., Shi P., and Zhang J. Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol 24 (2007) 2153-2157
35. Grus W.E., and Zhang J. Distinct evolutionary patterns between chemoreceptors of 2 vertebrate olfactory systems and the differential tuning hypothesis. Mol Biol Evol 25 (2008) 1593-1601
36. Hagino-Yamagishi K., Moriya K., Kubo H., Wakabayashi Y., Isobe N., Saito S., et al. Expression of vomeronasal receptor genes in Xenopus laevis. J Comp Neurol 472 (2004) 246-256
37. Halpern M., and Martínez-Marcos A. Structure and function of the vomeronasal system: an update. Prog Neurobiol 70 (2003) 245-318
38. Hansen A., Anderson K.T., and Finger T.E. Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates. J Comp Neurol 477 (2004) 347-359
39. Herrada G., and Dulac C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90 (1997) 763-773
40. Hudson R., and Distel H. Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37 (1986) 123-128
41. Jacob S., McClintock M.K., Zelano B., and Ober C. Paternally inherited HLA alleles are associated with women's choice of male odor. Nat Genet 30 (2002) 175-179
42. Jemiolo B., Harvey S., and Novotny M. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc Natl Acad Sci USA 83 (1986) 4576-4579
43. Karlson P., and Luscher M. 'Pheromones': a new term for a class of biologically active substances. Nature 183 (1959) 55-56
44. Keller M., Douhard Q., Baum M.J., and Bakker J. Sexual experience does not compensate for the disruptive effects of zinc sulfate-lesioning of the main olfactory epithelium on sexual behavior in male mice. Chem Senses 31 (2006) 753-762
45. Keller M., Pierman S., Douhard Q., Baum M.J., and Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur J Neurosci 23 (2006) 521-530
46. Kelliher K.R., Spehr M., Li X.H., Zufall F., and Leinders-Zufall T. Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur J Neurosci 23 (2006) 3385-3390
47. Keverne E.B. Pheromonal influences on the endocrine regulation of reproduction. Trends Neurosci 6 (1983) 381
48. Keverne E.B., Martel F.L., and Nevison C.M. Primate brain evolution: genetic and functional considerations. Proc R Soc Lond B: Biol Sci 263 (1996) 689-696
49. Keverne E.B. The vomeronasal organ. Science 286 (1999) 716-720
50. Keverne E.B. Brain evolution, chemosensory processing, and behavior. Nutr Rev 62 (2004) S218-S223 [discussion S224-41]
51. Kikuyama S., Toyoda F., Ohmiya Y., Matsuda K., Tanaka S., and Hayashi H. Sodefrin: a female-attracting peptide pheromone in newt cloacal glands. Science 267 (1995) 1643-1645
52. Kikuyama S., Yamamoto K., Iwata T., and Toyoda F. Peptide and protein pheromones in amphibians. Comp Biochem Physiol Part B: Biochem Mol Biol 132 (2002) 69-74
53. Kikuyama S., Nakada T., Toyoda F., Iwata T., Yamamoto K., and Conlon J.M. Amphibian pheromones and endocrine control of their secretion. Ann N Y Acad Sci 1040 (2005) 123-130
54. Laberge F., Feldhoff R.C., Feldhoff P.W., and Houck L.D. Courtship pheromone-induced c-Fos-like immunolabeling in the female salamander brain. Neuroscience 151 (2008) 329-339
55. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., et al. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405 (2000) 792-796
56. Leinders-Zufall T., Brennan P., Widmayer P.S.P.C., Maul-Pavicic A., Jager M., Li X.H., et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306 (2004) 1033-1037
57. Liberles S.D., and Buck L.B. A second class of chemosensory receptors in the olfactory epithelium. Nature 442 (2006) 645-650
58. Liman E.R., and Innan H. Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100 (2003) 3328-3332
59. Lin D.Y., Zhang S.-Z., Block E., and Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 434 (2005) 470-477
60. Lloyd-Thomas A., and Keverne E.B. Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience 7 (1982) 907-913
61. Luo M., Fee M.S., and Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299 (2003) 1196-1201
62. Mackay-Sim A., Duvall D., and Graves B.M. The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ. Brain Behav Evol 27 (1985) 186-194
63. Mandiyan V.S., Coats J.K., and Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat Neurosci 8 (2005) 1660-1662
64. Matsunami H., and Buck L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90 (1997) 775-784
65. Meisami E., and Bhatnagar K.P. Structure and diversity in mammalian accessory olfactory bulb. Microsc Res Tech 43 (1998) 476-499
66. Meredith M. Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol Behav 36 (1986) 737-743
67. Meredith M. Chronic recording of vomeronasal pump activation in awake behaving hamsters. Physiol Behav 56 (1994) 345-354
68. Moreno N., and Gonzalez A. Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transition. J Anat 211 (2007) 151-163
69. Niimura Y., and Nei M. Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51 (2006) 505-517
70. Novotny M., Harvey S., Jemiolo B., and Alberts J. Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci USA 82 (1985) 2059-2061
71. Powers J.B., and Winans S.S. Vomeronasal organ: critical role in mediating sexual behavior of the male hamster. Science 187 (1975) 961-963
72. Preti G., Wysocki C.J., Barnhart K.T., Sondheimer S.J., and Leyden J.J. Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol Reprod 68 (2003) 2107-2113
73. Rodriguez I., and Mombaerts P. Novel human vomeronasal receptor-like genes reveal species-specific families. Curr Biol 12 (2002) R409-R411
74. Rollmann S.M., Houck L.D., and Feldhoff R.C. Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science 285 (1999) 1907-1909
75. Ryba N.J., and Tirindelli R. A new multigene family of putative pheromone receptors. Neuron 19 (1997) 371-379
76. Schaal B., Coureaud G., Langlois D., Ginies C., Semon E., and Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424 (2003) 68-72
77. Shi P., and Zhang J. Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res 17 (2007) 166-174
78. Spehr M., Kelliher K.R., Li X.H., Boehm T., Leinders-Zufall T., and Zufall F. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26 (2006) 1961-1970
79. Stern K., and McClintock M.K. Regulation of ovulation by human pheromones. Nature 392 (1998) 177-179
80. Stowers L., Holy T.E., Meister M., Dulac C., and Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295 (2002) 1493-1500
81. Surridge A.K., Osorio D., and Mundy N.I. Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18 (2003) 198-205
82. Swanson L.W., and Petrovich G.D. What is the amygdala?. Trends Neurosci 21 (1998) 323-331
83. von Campenhausen H., and Mori K. Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur J Neurosci 12 (2000) 33-46
84. Wabnitz P.A., Bowie J.H., Tyler M.J., Wallace J.C., and Smith B.P. Differences in the skin peptides of the male and female Australian tree frog Litoria splendida. Eur J Biochem 267 (2000) 269-275
85. Wible J.R., and Bhatnagar K.P. Chiropteran vomeronasal complex and the interfamilial relationships of bats. J Mamm Evol 3 (1996) 285-314
86. Wirsig-Wiechmann C.R., Houck L.D., Feldhoff P.W., and Feldhoff R.C. Pheromonal activation of vomeronasal neurons in plethodontid salamanders. Brain Res 952 (2002) 335-344
87. Xu F., Schaefer M., Kida I., Schafer J., Liu N., Rothman D.L., et al. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol 489 (2005) 491-500
88. Yamamoto K., Kawai Y., Hayashi T., Ohe Y., Hayashi H., Toyoda F., et al. Silefrin, a sodefrin-like pheromone in the abdominal gland of the sword-tailed newt, Cynops ensicauda. FEBS Lett 472 (2000) 267-270
89. Young J.M., Kambere M., Trask B.J., and Lane R.P. Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res 15 (2005) 231-240
90. Young J.M., and Trask B.J. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23 (2007) 212-215
91. Zhang J., and Webb D.M. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100 (2003) 8337-8341