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

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 196, Issue 10, 2010, Pages 685-700

  Wyatt, Tristram D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Behavior; Individuality; Learning; Pheromone; Recognition; Signature mixture

Indexed keywords

PHEROMONE;

ANIMAL; ANIMAL COMMUNICATION; ASSOCIATION; COMPARATIVE STUDY; FEMALE; HUMAN; INVERTEBRATE; MALE; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPECIES DIFFERENCE; VERTEBRATE;

ANIMAL COMMUNICATION; ANIMALS; CUES; FEMALE; HUMANS; INVERTEBRATES; MALE; PHEROMONES; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; VERTEBRATES;

EID: 77957156136     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-010-0564-y     Document Type: Review

References (136)

1. Alberts AC (1989) Ultraviolet visual sensitivity in desert iguanas-implications for pheromone detection. Anim Behav 38: 129-137.
2. Altstein M (2004) Peptide pheromones: an overview. Peptides 25: 1373-1376. doi: 10. 1016/j. peptides. 2004. 07. 002.
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: 1-11.
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 115-144.
5. Bateson P, Mameli M (2007) The innate and the acquired: useful clusters or a residual distinction from folk biology? Dev Psychobiol 49: 818-831.
6. Baum MJ, Kelliher KR (2009) Complementary roles of the main and accessory olfactory systems in mammalian mate recognition. Annu Rev Physiol 71: 141-160.
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 143-160.
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: 713-731.
9. Benton R (2009) Molecular basis of odor detection in insects. Ann N Y Acad Sci 1170: 478-481.
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.
11. Beynon RJ, Hurst JL (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31: 142-146.
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.
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 57-78.
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, Cambridge.
15. Breithaupt T, Thiel M (eds) (2010) Chemical communication in crustaceans. Springer, New York.
16. Brennan PA (2009) Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice. Behav Brain Res 200: 287-294.
17. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Phil Trans R Soc B 361: 2061-2078.
18. Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444: 308-315.
19. de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34: 882-897.
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 283-332.
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: 899-902.
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.
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.
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 201-232.
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 248-282.
27. d'Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15: 2170-2174.
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 81-96.
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: 473-477.
30. Dawkins R (1976) The selfish gene. Oxford University Press, Oxford.
31. Døving KB, Lastein S (2009) The alarm reaction in fishes - odorants, modulations of responses, neural pathways. Ann N Y Acad Sci 1170: 413-423.
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 341-368.
33. Eisthen HL (2002) Why are olfactory systems of different animals so similar? Brain Behav Evol 59: 273-293.
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: 1845-1864.
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: 1844-1848.
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: 347-353.
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: 2091-2110.
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.
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.
40. Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124: 741-761.
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.
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.
43. Hamilton WD (1964) The genetical evolution of social behaviour. I and II. J Theor Biol 7: 1-32.
44. Hansson BS (2002) A bug's smell-research into insect olfaction. Trends Neurosci 25: 270-274.
45. Hasemeyer M, Yapici N, Heberlein U, Dickson BJ (2009) Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61: 511-518.
46. He J, Ma LM, Kim S, Nakai J, Yu CR (2008) Encoding gender and individual information in the mouse vomeronasal organ. Science 320: 535-538.
47. Hensch T (2004) Critical period regulation. Annu Rev Neurosci 27: 549-579.
48. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595-631.
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: 567-581.
50. Houck LD (2009) Pheromone communication in amphibians and reptiles. Annu Rev Physiol 71: 161-176.
51. Houck LD, Reagan NL (1990) Male courtship pheromones increase female receptivity in a plethodontid salamander. Anim Behav 39: 729-734.
52. Hudson R (1993) Olfactory imprinting. Curr Opin Neurobiol 3: 548-552.
53. Hudson R, Distel H (1986) Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37: 123-128.
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: 55-81.
55. Hurst JL (2009) Female recognition and assessment of males through scent. Behav Brain Res 200: 295-303.
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: 1187-1203.
57. Johnson ME, Atema J (2005) The olfactory pathway for individual recognition in the American lobster Homarus americanus. J Exp Biol 208: 2865-2872.
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: 1141-1162.
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 269-282.
61. Karlson P, Lüscher M (1959) 'Pheromones': a new term for a class of biologically active substances. Nature 183: 55-56.
62. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11: 188-200. doi: 10. 1038/nrn2789.
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: 268-276.
64. Kelly DR (1996) When is a butterfly like an elephant? Chem Biol 3: 595-602.
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: 1879-1884.
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 195-219.
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.
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: 323-326.
69. Koene JM, ter Maat A (2002) The distinction between pheromones and allohormones-reply. J Comp Physiol A Sens Neural Behav Physiol 188: 163-164.
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.
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.
73. Lazar J, Rasmussen LEL, Greenwood DR, Bang IS, Prestwich GD (2004) Elephant albumin: a multipurpose pheromone shuttle. Chem Biol 11: 1093-1100.
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.
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: 792-796.
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: 1033-1037.
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.
78. Lenoir A, d'Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46: 573-599.
79. Lévy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200: 336-345.
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 254-281.
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.
82. Lin DY, Zhang SZ, Block E, Katz LC (2005) Encoding social signals in the mouse main olfactory bulb. Nature 434: 470-477.
83. Lin DY, Shea SD, Katz LC (2006) Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50: 937-949.
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.
85. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96: 713-723.
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.
87. Mason RT (1993) Chemical ecology of the red-sided garter snake, Thamnophis sirtalis parietalis. Brain Behav Evol 41: 261-268.
88. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford.
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: 167-176.
90. Munger SD, Leinders-Zufall T, Zufall F (2009) Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71: 115-140.
91. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19: 284-292.
92. Novotny MV (2003) Pheromones, binding proteins and receptor responses in rodents. Biochem Soc Trans 31: 117-122.
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: 2059-2061.
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: 311-314.
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: 622-628.
96. Rasmussen LEL, Lazar J, Greenwood DR (2003) Olfactory adventures of elephantine pheromones. Biochem Soc Trans 31: 137-141.
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.
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.
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: 161-162.
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: 323-335.
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.
102. Schaal B (2008) Social odors and pheromones in mammals. Biofutur 27: 41-45.
103. Schaal B, Porter RH (1991) Microsmatic humans revisited-the generation and perception of chemical signals. Adv Study Behav 20: 135-199.
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: 68-72.
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: 346-358.
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: 9513-9521.
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 69-96.
108. Sisler SP, Sorensen PW (2008) Common carp and goldfish discern conspecific identity using chemical cues. Behaviour 145: 1409-1425.
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: 1449.
110. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31: 2731-2745.
111. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102: 77-97.
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 15-48.
113. Sorensen PW, Christensen TA, Stacey NE (1998) Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr Opin Neurobiol 8: 458-467.
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 125-129.
115. Spehr M, Munger SD (2009) Olfactory receptors: G protein-coupled receptors and beyond. J Neurochem 109: 1570-1583.
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.
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 359-412.
118. Strausfeld NJ, Hildebrand JG (1999) Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9: 634-639.
119. Su CY, Menuz K, Carlson JR (2009) Olfactory perception: receptors, cells, and circuits. Cell 139: 45-59.
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: 530-535.
121. Tibbetts EA, Dale J (2007) Individual recognition: It is good to be different. Trends Ecol Evol 22: 529-537.
122. Touhara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71: 307-332.
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 222-243.
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.
125. Vosshall LB, Stocker RE (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30: 505-533.
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: 833-841.
127. Wilson EO (1970) Chemical communication within animal species. In: Sondheimer E (ed) Chemical ecology, vol 9. Academic Press, New York, pp 133-155.
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 423-444.
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, Cambridge.
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 7-20.
132. Wyatt TD (2009) Fifty years of pheromones. Nature 457: 262-263.
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: 4467-4472.
134. Yamagata N, Nishino H, Mizunami M (2006) Pheromone-sensitive glomeruli in the primary olfactory centre of ants. Proc R Soc B 273: 2219-2225.
135. Yamagata N, Nishino H, Mizunami M (2007) Neural pathways for the processing of alarm pheromone in the ant brain. J Comp Neurol 505: 424-442.
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.