Journal of Comparative Physiology A

, Volume 196, Issue 10, pp 685–700 | Cite as

Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates

  • Tristram D. WyattEmail author


Pheromones have been found in species in almost every part of the animal kingdom, including mammals. Pheromones (a molecule or defined combination of molecules) are species-wide signals which elicit innate responses (though responses can be conditional on development as well as context, experience, and internal state). In contrast, signature mixtures, in invertebrates and vertebrates, are variable subsets of molecules of an animal’s chemical profile which are learnt by other animals, allowing them to distinguish individuals or colonies. All signature mixtures, and almost all pheromones, whatever the size of molecules, are detected by olfaction (as defined by receptor families and glomerular processing), in mammals by the main olfactory system or vomeronasal system or both. There is convergence on a glomerular organization of olfaction. The processing of all signature mixtures, and most pheromones, is combinatorial across a number of glomeruli, even for some sex pheromones which appear to have ‘labeled lines’. Narrowly specific pheromone receptors are found, but are not a prerequisite for a molecule to be a pheromone. A small minority of pheromones act directly on target tissues (allohormone pheromones) or are detected by non-glomerular chemoreceptors, such as taste. The proposed definitions for pheromone and signature mixture are based on the heuristic value of separating these kinds of chemical information. In contrast to a species-wide pheromone, there is no single signature mixture to find, as signature mixtures are a ‘receiver-side’ phenomenon and it is the differences in signature mixtures which allow animals to distinguish each other.


Pheromone Signature mixture Behavior Recognition Learning Individuality 





Accessory olfactory bulb


Accessory olfactory system


cis-Vinyl acetate




Exocrine gland-secreting peptide 1


Gas chromatography


High-performance liquid chromatography


Major histocompatibility complex


Main olfactory epithelium


Main olfactory system


Medial olfactory tract




Major urinary protein


Olfactory receptor protein


Olfactory sensory neuron




Vomeronasal organ


Vomeronasal system


Vomeronasal receptor protein



I thank two anonymous referees for their helpful comments, and PB Brennan, P d’Ettorre, M De Facci and Lund colleagues, J Kwak, and PW Sorensen, for their contributions and comments on a draft of this paper. Ethical standards: Review n/a.

Conflict of interest

The author declares that he has no conflict of interest.


  1. Alberts AC (1989) Ultraviolet visual sensitivity in desert iguanas—implications for pheromone detection. Anim Behav 38:129–137Google Scholar
  2. Altstein M (2004) Peptide pheromones: an overview. Peptides 25:1373–1376. doi: 10.1016/j.peptides.2004.07.002 PubMedGoogle Scholar
  3. Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl 123:1–11Google Scholar
  4. Atema J, Steinbach MA (2007) Chemical communication and social behavior of the lobster Homarus americanus and other decapod Crustacea. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, Oxford & New York, pp 115–144Google Scholar
  5. Bateson P, Mameli M (2007) The innate and the acquired: useful clusters or a residual distinction from folk biology? Dev Psychobiol 49:818–831PubMedGoogle Scholar
  6. Baum MJ, Kelliher KR (2009) Complementary roles of the main and accessory olfactory systems in mammalian mate recognition. Annu Rev Physiol 71:141–160PubMedGoogle Scholar
  7. Beauchamp GK, Doty RL, Moulton DG, Mugford RA (1976) The pheromone concept in mammalian chemical communication: a critique. In: Doty RL (ed) Mammalian olfaction, reproductive processes, and behavior. Academic Press, New York, pp 143–160Google Scholar
  8. Belanger RM, Moore PA (2006) The use of the major chelae by reproductive male crayfish (Orconectes rusticus) for discrimination of female odours. Behaviour 143:713–731Google Scholar
  9. Benton R (2009) Molecular basis of odor detection in insects. Ann N Y Acad Sci 1170:478–481PubMedGoogle Scholar
  10. Ben-Shaul Y, Katz LC, Mooney R, Dulac C (2010) In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. Proc Natl Acad Sci USA 107:5172–5177. doi: 10.1073/pnas.0915147107 Google Scholar
  11. Beynon RJ, Hurst JL (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31:142–146PubMedGoogle Scholar
  12. Boehm T, Zufall F (2006) MHC peptides and the sensory evaluation of genotype. Trends Neurosci 29:100–107. doi: 10.1016/j.tins.2005.11.006 PubMedGoogle Scholar
  13. Breed MD (1998) Chemical cues in kin recognition: criteria for identification, experimental approaches, and the honey bee as an example. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview Press, Boulder, pp 57–78Google Scholar
  14. Breed MD, Buchwald R (2009) Cue diversity and social recognition. In: Gadau J, Fewell JH (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, CambridgeGoogle Scholar
  15. Breithaupt T, Thiel M (eds) (2010) Chemical communication in crustaceans. Springer, New YorkGoogle Scholar
  16. Brennan PA (2009) Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice. Behav Brain Res 200:287–294PubMedGoogle Scholar
  17. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Phil Trans R Soc B 361:2061–2078PubMedGoogle Scholar
  18. Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315PubMedGoogle Scholar
  19. de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897PubMedGoogle Scholar
  20. Cardé RT, Haynes KF (2004) Structure of the pheromone communication channel in moths In: Cardé R, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 283–332Google Scholar
  21. Caro S, Balthazart J (2010) Pheromones in birds: myth or reality? J Comp Physiol A Sens Neural Behav Physiol. doi: 10.1007/s00359-010-0534-4
  22. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899–902PubMedGoogle Scholar
  23. Christensen TA (2005) Making scents out of spatial and temporal codes in specialist and generalist olfactory networks. Chem Senses 30:i283–i284. doi: 10.1093/chemse/bjh225 PubMedGoogle Scholar
  24. Christensen TA, Hildebrand JG (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12:393–399. doi: 10.1016/s0959-4388(02)00336-7 PubMedGoogle Scholar
  25. Christensen TA, White J (2000) Representation of olfactory information in the brain. In: Finger TE, Silver WL, Restrepo D (eds) The neurobiology of taste and smell, 2nd edn. Wiley-Liss, New York, pp 201–232Google Scholar
  26. Conner W, Weller S (2004) A quest for alkaloids: the curious relationship between tiger moths and plants containing pyrrolizidine alkaloids. In: Cardé R, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 248–282Google Scholar
  27. d’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174PubMedGoogle Scholar
  28. d’Ettorre P, Moore AJ (2008) Chemical communication and the coordination of social interactions in insects. In: d’Ettorre P, Hughes DP (eds) Sociobiology of communication: an interdisciplinary perspective. Oxford University Press, Oxford, pp 81–96Google Scholar
  29. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452:473–477PubMedGoogle Scholar
  30. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  31. Døving KB, Lastein S (2009) The alarm reaction in fishes - odorants, modulations of responses, neural pathways. Ann N Y Acad Sci 1170:413–423PubMedGoogle Scholar
  32. Eisner T, Meinwald J (2003) Alkaloid-derived pheromones and sexual selection in Lepidoptera. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology: the biosynthesis and detection of insect pheromones and plant volatiles. Academic Press, New York, pp 341–368Google Scholar
  33. Eisthen HL (2002) Why are olfactory systems of different animals so similar? Brain Behav Evol 59:273–293PubMedGoogle Scholar
  34. Ekerholm M, Hallberg E (2005) Primer and short-range releaser pheromone properties of premolt female urine from the shore crab Carcinus maenas. J Chem Ecol 31:1845–1864PubMedGoogle Scholar
  35. Eltz T, Zimmermann Y, Pfeiffer C, Pech J, Twele R, Francke W, Quezada-Euan J, Lunau K (2008) An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol 18:1844–1848PubMedGoogle Scholar
  36. Ferkin MH, Sorokin ES, Renfroe MW, Johnston RE (1994) Attractiveness of male odors to females varies directly with plasma testosterone concentration in meadow voles. Physiol Behav 55:347–353PubMedGoogle Scholar
  37. Fine JM, Vrieze LA, Sorensen PW (2004) Evidence that petromyzontid lampreys employ a common migratory pheromone that is partially comprised of bile acids. J Chem Ecol 30:2091–2110PubMedGoogle Scholar
  38. Gotzek D, Ross KG (2009) Current status of a model system: the gene Gp-9 and its association with social organization in fire ants. PLoS ONE 4:e7713. doi: 10.1371/journal.pone.0007713 PubMedGoogle Scholar
  39. Haga S, Hattori T, Sato T, Sato K, Matsuda S, Kobayakawa R, Sakano H, Yoshihara Y, Kikusui T, Touhara K (2010) The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 466:118–123. doi: 10.1038/nature09142 PubMedGoogle Scholar
  40. Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124:741–761Google Scholar
  41. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160. doi: 10.1016/j.cell.2006.01.050 PubMedGoogle Scholar
  42. Hamdani EH, Døving KB (2007) The functional organization of the fish olfactory system. Prog Neurobiol 82:80–86. doi: 10.1016/j.pneurobio.2007.02.007 Google Scholar
  43. Hamilton WD (1964) The genetical evolution of social behaviour. I and II. J Theor Biol 7:1–32PubMedGoogle Scholar
  44. Hansson BS (2002) A bug’s smell—research into insect olfaction. Trends Neurosci 25:270–274PubMedGoogle Scholar
  45. Hasemeyer M, Yapici N, Heberlein U, Dickson BJ (2009) Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61:511–518PubMedGoogle Scholar
  46. He J, Ma LM, Kim S, Nakai J, Yu CR (2008) Encoding gender and individual information in the mouse vomeronasal organ. Science 320:535–538PubMedGoogle Scholar
  47. Hensch T (2004) Critical period regulation. Annu Rev Neurosci 27:549–579PubMedGoogle Scholar
  48. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631PubMedGoogle Scholar
  49. Hölldobler B, Carlin NF (1987) Anonymity and specificity in the chemical communication signals of social insects. J Comp Physiol A Sens Neural Behav Physiol 161:567–581Google Scholar
  50. Houck LD (2009) Pheromone communication in amphibians and reptiles. Annu Rev Physiol 71:161–176PubMedGoogle Scholar
  51. Houck LD, Reagan NL (1990) Male courtship pheromones increase female receptivity in a plethodontid salamander. Anim Behav 39:729–734Google Scholar
  52. Hudson R (1993) Olfactory imprinting. Curr Opin Neurobiol 3:548–552PubMedGoogle Scholar
  53. Hudson R, Distel H (1986) Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37:123–128PubMedGoogle Scholar
  54. Hurst JL (1993) The priming effects of urine substrate marks on interactions between male house mice, Mus musculus domesticus Schwarz and Schwarz. Anim Behav 45:55–81Google Scholar
  55. Hurst JL (2009) Female recognition and assessment of males through scent. Behav Brain Res 200:295–303PubMedGoogle Scholar
  56. Jefferis GSXE, Potter CJ, Chan AI, Marin EC, Rohlfing T, Maurer CR, Luo LQ (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203PubMedGoogle Scholar
  57. Johnson ME, Atema J (2005) The olfactory pathway for individual recognition in the American lobster Homarus americanus. J Exp Biol 208:2865–2872PubMedGoogle Scholar
  58. Johnson NS, Li W (2010) Understanding behavioral responses of fish to pheromones in natural freshwater environments. J Comp Physiol A Sens Neural Behav Physiol. doi: 10.1007/s00359-010-0523-7
  59. Johnston RE (2003) Chemical communication in rodents: from pheromones to individual recognition. J Mammal 84:1141–1162Google Scholar
  60. Johnston RE (2005) Communication by mosaic signals: individual recognition and underlying neural mechanisms. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol 10. Springer, New York, pp 269–282Google Scholar
  61. Karlson P, Lüscher M (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183:55–56PubMedGoogle Scholar
  62. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200. doi: 10.1038/nrn2789 PubMedGoogle Scholar
  63. Keller M, Baum MJ, Brock O, Brennan PA, Bakker J (2009) The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav Brain Res 200:268–276PubMedGoogle Scholar
  64. Kelly DR (1996) When is a butterfly like an elephant? Chem Biol 3:595–602PubMedGoogle Scholar
  65. Kimoto H, Sato K, Nodari F, Haga S, Holy TE, Touhara K (2007) Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr Biol 17:1879–1884PubMedGoogle Scholar
  66. Kleineidam CJ, Rossler W (2009) Adaptations in the olfactory system of social Hymenoptera. In: Gadau J, Fewell JH (eds) Organization of insect societies: from genome to sociocomplexity. Harvard Univ Press, Cambridge, pp 195–219Google Scholar
  67. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503–508. doi: 10.1038/nature06281 PubMedGoogle Scholar
  68. Koene JM, ter Maat A (2001) “Allohormones”: a class of bioactive substances favoured by sexual selection. J Comp Physiol A Sens Neural Behav Physiol 187:323–326Google Scholar
  69. Koene JM, ter Maat A (2002) The distinction between pheromones and allohormones—reply. J Comp Physiol A Sens Neural Behav Physiol 188:163–164Google Scholar
  70. Kristoffersen L, Hansson BS, Anderbrant O, Larsson MC (2008) Aglomerular hemipteran antennal lobes–basic neuroanatomy of a small nose. Chem Senses 33:771–778. doi: 10.1093/chemse/bjn044 PubMedGoogle Scholar
  71. Kwak J, Willse A, Preti G, Yamazaki K, Beauchamp G (2010) In search of the chemical basis for MHC odourtypes. Proc R Soc B. doi: 10.1098/rspb.2010.0162
  72. Lassance JM, Löfstedt C (2009) Concerted evolution of male and female display traits in the European corn borer, Ostrinia nubilalis. BMC Biol 7:10. doi: 10.1186/1741-7007-7-10 PubMedGoogle Scholar
  73. Lazar J, Rasmussen LEL, Greenwood DR, Bang IS, Prestwich GD (2004) Elephant albumin: a multipurpose pheromone shuttle. Chem Biol 11:1093–1100PubMedGoogle Scholar
  74. Leal WS, Ishida Y (2008) GP-9 s are ubiquitous proteins unlikely involved in olfactory mediation of social organization in the red imported fire ant, Solenopsis invicta. PLoS ONE 3:e3762. doi: 10.1371/journal.pone.0003762 PubMedGoogle Scholar
  75. Leinders-Zufall T, Lane AP, Puche AC, Ma WD, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796PubMedGoogle Scholar
  76. Leinders-Zufall T, Brennan P, Widmayer P, Chandramani P, 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 306:1033–1037PubMedGoogle Scholar
  77. Leinders-Zufall T, Ishii T, Mombaerts P, Zufall F, Boehm T (2009) Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides. Nat Neurosci 12:1551–1558. doi: 10.1038/nn.2452 PubMedGoogle Scholar
  78. Lenoir A, d’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599PubMedGoogle Scholar
  79. Lévy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200:336–345PubMedGoogle Scholar
  80. Liebig J (2010) Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 254–281Google Scholar
  81. Liénard MA, Strandh M, Hedenstrom E, Johansson T, Löfstedt C (2008) Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol Biol 8:270. doi: 10.1186/1471-2148-8-270 PubMedGoogle Scholar
  82. Lin DY, Zhang SZ, Block E, Katz LC (2005) Encoding social signals in the mouse main olfactory bulb. Nature 434:470–477PubMedGoogle Scholar
  83. Lin DY, Shea SD, Katz LC (2006) Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50:937–949Google Scholar
  84. Logan DW, Marton TF, Stowers L (2008) Species specificity in major urinary proteins by parallel evolution. PLoS ONE 3:e3280. doi: 10.1371/journal.pone.0003280 PubMedGoogle Scholar
  85. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723PubMedGoogle Scholar
  86. Martín J, López P (2010) Condition-dependent pheromone signaling by male rock lizards: more oily scents are more attractive. Chem Senses 35:253–262. doi: 10.1093/chemse/bjq009 PubMedGoogle Scholar
  87. Mason RT (1993) Chemical ecology of the red-sided garter snake, Thamnophis sirtalis parietalis. Brain Behav Evol 41:261–268PubMedGoogle Scholar
  88. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  89. Moncho-Bogani J, Lanuza E, Hernandez A, Novejarque A, Martinez-Garcia F (2002) Attractive properties of sexual pheromones in mice: innate or learned? Physiol Behav 77:167–176PubMedGoogle Scholar
  90. Munger SD, Leinders-Zufall T, Zufall F (2009) Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71:115–140PubMedGoogle Scholar
  91. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19:284–292PubMedGoogle Scholar
  92. Novotny MV (2003) Pheromones, binding proteins and receptor responses in rodents. Biochem Soc Trans 31:117–122PubMedGoogle Scholar
  93. Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci USA 82:2059–2061PubMedGoogle Scholar
  94. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314PubMedGoogle Scholar
  95. Peele P, Salazar I, Mimmack M, Keverne EB, Brennan PA (2003) Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. Eur J Neurosci 18:622–628PubMedGoogle Scholar
  96. Rasmussen LEL, Lazar J, Greenwood DR (2003) Olfactory adventures of elephantine pheromones. Biochem Soc Trans 31:137–141PubMedGoogle Scholar
  97. Restrepo D, Lin WH, Salcedo E, Yarnazaki K, Beauchamp G (2006) Odortypes and MHC peptides: complementary chemosignals of MHC haplotype? Trends Neurosci 29:604–609. doi: 10.1016/j.tins.2006.08.001 PubMedGoogle Scholar
  98. Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. BMC Biol 8:75. doi: 10.1186/1741-7007-8-75 PubMedGoogle Scholar
  99. Ruther J, Steidle JLM (2002) “Allohormones”: a new class of bioactive substances or old wine in new skins? J Comp Physiol A Sens Neural Behav Physiol 188:161–162Google Scholar
  100. Sanchez-Andrade G, Kendrick KM (2009) The main olfactory system and social learning in mammals: Pheromonal communication in higher vertebrates and its implication for reproductive function. Behav Brain Res 200:323–335PubMedGoogle Scholar
  101. Sandoz JC, Deisig N, de Brito Sanchez MG, Giurfa M (2007) Understanding the logics of pheromone processing in the honeybee brain: from labeled-lines to across-fiber patterns. Front Behav Neurosci 1:5. doi: 10.3389/neuro.08.005.2007 PubMedGoogle Scholar
  102. Schaal B (2008) Social odors and pheromones in mammals. Biofutur 27:41–45Google Scholar
  103. Schaal B, Porter RH (1991) Microsmatic humans revisited—the generation and perception of chemical signals. Adv Study Behav 20:135–199Google Scholar
  104. Schaal B, Coureaud G, Langlois D, Ginies C, Semon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68–72PubMedGoogle Scholar
  105. Schaal B, Coureaud G, Doucet S, Delaunay-El Allam M, Moncomble A-S, Montigny D, Patris B, Holley A (2009) Mammary olfactory signalisation in females and odor processing in neonates: ways evolved by rabbits and humans. Behav Brain Res 200:346–358PubMedGoogle Scholar
  106. Schaefer ML, Yamazaki K, Osada K, Restrepo D, Beauchamp GK (2002) Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition, and behavior. J Neurosci 22:9513–9521PubMedGoogle Scholar
  107. Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell Science, Oxford, pp 69–96Google Scholar
  108. Sisler SP, Sorensen PW (2008) Common carp and goldfish discern conspecific identity using chemical cues. Behaviour 145:1409–1425Google Scholar
  109. Slagsvold T, Hansen B, Johannessen L, Lifjeld J (2002) Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc R Soc Lond B Biol Sci 269:1449Google Scholar
  110. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745Google Scholar
  111. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97PubMedGoogle Scholar
  112. Sorensen PW, Stacey NE (1999) Evolution and specialization of fish hormonal pheromones. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Kluwer Academic/Plenum Press, New York, pp 15–48Google Scholar
  113. Sorensen PW, Christensen TA, Stacey NE (1998) Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr Opin Neurobiol 8:458–467PubMedGoogle Scholar
  114. Sorensen PW, Scott AP, Kihslinger RL (2000) How common hormonal metabolites function as specific pheromones in the goldfish. In: Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds) Proceedings of the sixth international symposium on the reproductive physiology of fish. Bergen, Norway, pp 125–129Google Scholar
  115. Spehr M, Munger SD (2009) Olfactory receptors: G protein-coupled receptors and beyond. J Neurochem 109:1570–1583PubMedGoogle Scholar
  116. Spehr M, Kelliher KR, Li XH, Boehm T, Leinders-Zufall T, Zufall F (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26:1961–1970. doi: 10.1523/jneurosci.4939-05.2006 PubMedGoogle Scholar
  117. Stacey NE, Sorensen PW (2006) Reproductive pheromones. In: Sloman KA, Wilson RW, Balshine S (eds) Fish physiology, vol 24: Behaviour and physiology of fish. Academic Press, Elsevier, pp 359–412Google Scholar
  118. Strausfeld NJ, Hildebrand JG (1999) Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9:634–639PubMedGoogle Scholar
  119. Su CY, Menuz K, Carlson JR (2009) Olfactory perception: receptors, cells, and circuits. Cell 139:45–59PubMedGoogle Scholar
  120. Teicher MH, Stewart WB, Kauer JS, Shepherd GM (1980) Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory-bulb revealed by the 2-deoxyglucose method. Brain Res 194:530–535PubMedGoogle Scholar
  121. Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537PubMedGoogle Scholar
  122. Touhara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71:307–332PubMedGoogle Scholar
  123. van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 222–243Google Scholar
  124. Vergoz V, McQuillan HJ, Geddes LH, Pullar K, Nicholson BJ, Paulin MG, Mercer AR (2009) Peripheral modulation of worker bee responses to queen mandibular pheromone. Proc Natl Acad Sci USA 106:20930–20935. doi: 10.1073/pnas.0907563106 PubMedGoogle Scholar
  125. Vosshall LB, Stocker RE (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533PubMedGoogle Scholar
  126. Wang SP, Sato K, Giurfa M, Zhang SW (2008) Processing of sting pheromone and its components in the antennal lobe of the worker honeybee. J Insect Physiol 54:833–841PubMedGoogle Scholar
  127. Wilson EO (1970) Chemical communication within animal species. In: Sondheimer E (ed) Chemical ecology, vol 9. Academic Press, New York, pp 133–155Google Scholar
  128. Wood RI, Swann JM (2000) Neuronal integration of chemosensory and hormonal signals in the control of male sexual behavior. In: Wallen K, Schneider JE (eds) Reproduction in context: social and environmental influences on reproductive physiology and behavior. MIT Press, Cambridge, pp 423–444Google Scholar
  129. Woodley SK (2010) Pheromonal communication in amphibians. J Comp Physiol A Sens Neural Behav Physiol. doi: 10.1007/s00359-010-0540-6
  130. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, CambridgeGoogle Scholar
  131. Wyatt TD (2005) Pheromones: convergence and contrasts in insects and vertebrates. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol 10. Springer, New York, pp 7–20Google Scholar
  132. Wyatt TD (2009) Fifty years of pheromones. Nature 457:262–263PubMedGoogle Scholar
  133. Xue BY, Rooney AP, Kajikawa M, Okada N, Roelofs WL (2007) Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion. Proc Natl Acad Sci USA 104:4467–4472PubMedGoogle Scholar
  134. Yamagata N, Nishino H, Mizunami M (2006) Pheromone-sensitive glomeruli in the primary olfactory centre of ants. Proc R Soc B 273:2219–2225PubMedGoogle Scholar
  135. Yamagata N, Nishino H, Mizunami M (2007) Neural pathways for the processing of alarm pheromone in the ant brain. J Comp Neurol 505:424–442PubMedGoogle Scholar
  136. Zube C, Kleineidam CJ, Kirschner S, Neef J, Rossler W (2008) Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J Comp Neurol 506:425–441. doi: 10.1002/cne.21548 PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OxfordOxfordUK

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