Proteins and peptides as pheromone signals and chemical signatures

Animal Behaviour

Volumn 97, Issue , 2014, Pages 273-280

  Wyatt, Tristram D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Animal communication; Courtship; Mate choice; Multicomponent signal; Sex peptide; Sexual conflict; Sexual selection; Signal; Signalling; Signature mixture

Indexed keywords

AMPHIBIAN; CHEMICAL CUE; COURTSHIP; FLY; PEPTIDE; PHEROMONE; PROTEIN; RODENT; SEXUAL CONFLICT; SEXUAL SELECTION; SIGNAL; TERRITORIALITY;

ANIMALIA;

EID: 84908644898     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2014.07.025     Document Type: Article

References (100)

1. Archie E.A., Theis K.R. Animal behaviour meets microbial ecology. Animal Behaviour 2011, 82:425-436.
2. Arnqvist G. Sensory exploitation and sexual conflict. Philosophical Transactions of the Royal Society B: Biological Sciences 2006, 361:375-386.
3. Arnqvist G., Rowe L. Sexual conflict 2005, Princeton University Press, Princeton, NJ.
4. Avila F.W., Sirot L.K., Laflamme B.A., Rubinstein C.D., Wolfner M.F. Insect seminal fluid proteins: identification and function. Annual Review of Entomology 2011, 56:21-40.
5. Berg J.M., Tymoczko J.L., Stryer L. Biochemistry 2002, W. H. Freeman, New York, NY. 5th ed.
6. Beynon R.J., Armstrong S.D., Roberts S.A., Davidson A., Simpson D.M., Turton M.J., et al. The application of proteomics to the discovery and quantification of proteins in scent signals. Chemical signals in vertebrates 12 2013, 433-447. Springer, New York, NY. M.L. East, M. Dehnhard (Eds.).
7. Beynon R.J., Hurst J.L. Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 2004, 25:1553-1563.
8. Bocskei Z., Groom C.R., Flower D.R., Wright C.E., Phillips S.E.V., Cavaggioni A., et al. Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature 1992, 360:186-188.
9. Bradbury J.W., Vehrencamp S.L. Principles of animal communication 2011, Sinauer, Sunderland, MA. 2nded.
10. Breithaupt T., Hardege J. Pheromones mediating sex and dominance in aquatic animals. Chemical ecology in aquatic systems 2012, 39-56. Oxford University Press, Oxford, U.K. C. Brönmark, L.-A. Hansson (Eds.).
11. Brennan P.A. Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice. Behavioural Brain Research 2009, 200:287-294.
12. Buttstedt A., Moritz R.F., Erler S. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews 2014, 89:255-269.
13. Caskey J.L., Watson G.M., Bauer R.T. Studies on contact sex pheromones of the caridean shrimp Palaemonetes pugio: II. The role of glucosamine in mate recognition. Invertebrate Reproduction and Development 2009, 53:105-116.
14. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., et al. Identification of protein pheromones that promote aggressive behaviour. Nature 2007, 45:899-902.
15. Chapman T. The soup in my fly: evolution, form and function of seminal fluid proteins. PLoS Biology 2008, 6:e179.
16. Clare A.S. Toward a characterization of the chemical cue to barnacle gregariousness. Chemical communication in crustaceans 2011, 431-450. Springer, New York, NY. T. Breithaupt, M. Thiel (Eds.).
17. Cummins S.F., Boal J.G., Buresch K.C., Kuanpradit C., Sobhon P., Holm J.B., et al. Extreme aggression in male squid induced by a beta-MSP-like pheromone. Current Biology 2011, 21:322-327.
18. Cummins S.F., Xie F., de Vries M.R., Annangudi S.P., Misra M., Degnan B., et al. Aplysia temptin - the 'glue' in the water-borne attractin pheromone complex. FEBS Journal 2007, 274:5425-5437.
19. delBarco-Trillo J., Drea C.M. Socioecological and phylogenetic patterns in the chemical signals of strepsirrhine primates. Animal Behaviour 2014, 97:249-253.
20. 2 problem. Annual Review of Marine Science 2009, 1:169-192.
21. Doney S.C., Ruckelshaus M., Emmett Duffy J., Barry J.P., Chan F., English C.A., et al. Climate change impacts on marine ecosystems. Annual Review of Marine Science 2012, 4:11-37.
22. Drea C.M., Boulet M., Delbarco-Trillo J., Greene L.K., Sacha C.R., Goodwin T., et al. The 'secret' in secretions: methodological considerations in deciphering primate olfactory communication. American Journal of Primatology 2013, 75:621-642.
23. 2-macroglobulin-like protein is the cue to gregarious settlement of the barnacle Balanus amphitrite. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:14396-14401.
24. Drury J.P. Immunity and mate choice: a new outlook. Animal Behaviour 2010, 79:539-545.
25. Dusenbery D.B. Living at micro scale: The unexpected physics of being small 2009, Harvard University Press, Cambridge, MA.
26. Dusenbery D.B., Snell T.W. Acritical body size for use of pheromones in mate location. Journal of Chemical Ecology 1995, 21:427-438.
27. Eizaguirre C., Lenz T.L. Major histocompatability complex polymorphism: dynamics and consequences of parasite-mediated local adaptation in fishes. Journal of Fish Biology 2010, 77:2023-2047.
28. Ferrero D.M., Moeller L.M., Osakada T., Horio N., Li Q., Roy D.S., et al. Ajuvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system. Nature 2013, 502:368-371.
29. Forward R.B. Larval biology of the crab Rhithropanopeus harrisii (Gould): a synthesis. Biological Bulletin 2009, 216:243-256.
30. Ghaleb A., Atwood J., Morales-Montor J., Damian R. A3 kDa peptide is involved in the chemoattraction invitro of the male Schistosoma mansoni to the female. Microbes and Infection 2006, 8:2367-2375.
31. Good J.M., Wiebe V., Albert F.W., Burbano H.A., Kircher M., Green R.E., et al. Comparative population genomics of the ejaculate in humans and the great apes. Molecular Biology and Evolution 2013, 30:964-976.
32. Haga S., Hattori T., Sato T., Sato K., Matsuda S., Kobayakawa R., et al. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 2010, 466:118-122.
33. Hardege J.D., Bartels-Hardege H., Müller C.T., Beckmann M. Peptide pheromones in female Nereis succinea. Peptides 2004, 25:1517-1522.
34. Hardege J.D., Rotchell J.M., Terschak J., Greenway G.M. Analytical challenges and the development of biomarkers to measure and to monitor the effects of ocean acidification. Trends in Analytical Chemistry 2011, 30:1320-1326.
35. Häsemeyer M., Yapici N., Heberlein U., Dickson B.J. Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 2009, 61:511-518.
36. Havlíček J., Roberts S.C. MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 2009, 34:497-512.
37. Houck L.D. Pheromone communication in amphibians and reptiles. Annual Review of Physiology 2009, 71:161-176.
38. Hurst J.L., Beynon R.J. Rodent urinary proteins used in scent communication. Chemical signals in vertebrates 12 2013, 117-133. Springer, New York, NY. M.L. East, M. Dehnhard (Eds.).
39. Hurst J.L., Robertson D.H.L., Tolladay U., Beynon R.J. Proteins in urine scent Marks of male house mice extend the longevity of olfactory signals. Animal Behaviour 1998, 55:1289-1297.
40. Kamakura M. Royalactin induces queen differentiation in honeybees. Nature 2011, 473:478-483.
41. Karlson P., Lüscher M. 'Pheromones': a new term for a class of biologically active substances. Nature 1959, 183:55-56.
42. Karn R.C., Laukaitis C.M. Characterization of two forms of mouse salivary androgen-binding protein (ABP): implications for evolutionary relationships and ligand-binding function. Biochemistry 2003, 42:7162-7170.
43. Karn R.C., Laukaitis C.M. Selection shaped the evolution of mouse androgen-binding protein (ABP) function and promoted the duplication of Abp genes. Biochemical Society Transactions 2014, 42:851-860.
44. Kaupp U.B. Olfactory signalling in vertebrates and insects: differences and commonalities. Nature Reviews Neuroscience 2010, 11:188-200.
45. Kaur A.W., Ackels T., Kuo T.H., Cichy A., Dey S., Hays C., et al. Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 2014, 157:676-688.
46. Kimoto H., Haga S., Sato K., Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 2005, 437:898-901.
47. King J.D., Rollins-Smith L.A., Nielsen P.F., John A., Conlon J.M. Characterization of a peptide from skin secretions of male specimens of the frog, Leptodactylus fallax that stimulates aggression in male frogs. Peptides 2005, 26:597-601.
48. Koene J.M., ter Maat A. 'Allohormones': a class of bioactive substances favoured by sexual selection. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 2001, 187:323-326.
49. Koene J.M., ter Maat A. The distinction between pheromones and allohormones - reply. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 2002, 188:163-164.
50. Kwak J., Grigsby C.C., Rizki M.M., Preti G., Köksal M., Josue J., et al. Differential binding between volatile ligands and major urinary proteins due to genetic variation in mice. Physiology and Behavior 2012, 107:112-120.
51. Kwak J., Opiekun M.C., Matsumura K., Preti G., Yamazaki K., Beauchamp G.K. Major histocompatibility complex-regulated odortypes: peptide-free urinary volatile signals. Physiology and Behavior 2009, 96:184-188.
52. Laukaitis C., Karn R.C. Recognition of subspecies status mediated by androgen-binding protein (ABP) in the evolution of incipient reinforcement on the European house mouse hybrid zone. Evolution of the house mouse 2012, 150-190. Cambridge University Press, Cambridge, U.K. M. Macholan, P. Munclinger, S.J. Baird, J. Pialek (Eds.).
53. Leinders-Zufall T., Brennan P., Widmayer P., Chandramani P., Maul-Pavicic A., Jager M., et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306:1033-1037.
54. Logan D.W., Marton T.F., Stowers L. Species specificity in major urinary proteins by parallel evolution. PLoS One 2008, 3:e3280.
55. Matsuura K. Multifunctional queen pheromone and maintenance of reproductive harmony in termite colonies. Journal of Chemical Ecology 2012, 38:746-754.
56. Matsuura K., Tamura T., Kobayashi N., Yashiro T., Tatsumi S. The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLoS One 2007, 2:e813.
57. Matsuura K., Yashiro T., Shimizu K., Tatsumi S., Tamura T. Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme β-glucosidase. Current Biology 2009, 19:30-36.
58. Miklos G.L.G., Maleszka R. Epigenomic communication systems in humans and honey bees: from molecules to behavior. Hormones and Behavior 2011, 59:399-406.
59. Milinski M. The major histocompatibility complex, sexual selection, and mate choice. Annual Review of Ecology Evolution and Systematics 2006, 37:159-186.
60. Milinski M., Griffiths S., Wegner K.M., Reusch T.B.H., Haas-Assenbaum A., Boehm T. Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:4414-4418.
61. Mudge J.M., Armstrong S.D., McLaren K., Beynon R.J., Hurst J.L., Nicholson C., et al. Dynamic instability of the major urinary protein gene family revealed by genomic and phenotypic comparisons between C57 and 129 strain mice. Genome Biology 2008, 9:R91.
62. 8]sodefrin from the newt Cynops pyrrhogaster. Peptides 2007, 28:774-780.
63. Overath P., Sturm T., Rammensee H.G. Of volatiles and peptides: in search for MHC-dependent olfactory signals in social communication. Cellular and Molecular Life Sciences 2014, 71:2429-2442.
64. Palmer C.A., Watts R.A., Hastings A.P., Houck L.D., Arnold S.J. Rapid evolution of plethodontid modulating factor, a hypervariable salamander courtship pheromone, is driven by positive selection. Journal of Molecular Evolution 2010, 70:427-440.
65. Penn D.J. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 2002, 108:1-21.
66. Petrulis A. Chemosignals, hormones and mammalian reproduction. Hormones and Behavior 2013, 63:723-741.
67. Piertney S.B., Oliver M.K. The evolutionary ecology of the major histocompatibility complex. Heredity 2006, 96:7-21.
68. Poiani A. Complexity of seminal fluid: a review. Behavioral Ecology and Sociobiology 2006, 60:289-310.
69. Ramm S.A., McDonald L., Hurst J.L., Beynon R.J., Stockley P. Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Molecular Biology and Evolution 2009, 26:189-198.
70. Redaelli M., Orsetti A., Zagotto G., Cavaggioni A., Mucignat C. Airborne molecules released from male mouse urine affect female exploratory behavior. Frontiers in Ecology and Evolution 2014, 2:28.
71. Reisert J., Restrepo D. Molecular tuning of odorant receptors and its implication for odor signal processing. Chemical Senses 2009, 34:535-545.
72. Restrepo D., Lin W.H., Salcedo E., Yarnazaki K., Beauchamp G. Odortypes and MHC peptides: complementary chemosignals of MHC haplotype?. Trends in Neurosciences 2006, 29:604-609.
73. Rezával C., Pavlou H.J., Dornan A.J., Chan Y.-B., Kravitz E.A., Goodwin S.F. Neural circuitry underlying Drosophila female postmating behavioral responses. Current Biology 2012, 22:1155-1165.
74. Rittschof D., Cohen J.H. Crustacean peptide and peptide-like pheromones and kairomones. Peptides 2004, 25:1503-1516.
75. Roberts S.A., Davidson A.J., Beynon R.J., Hurst J.L. Female attraction to male scent and associative learning: the house mouse as a mammalian model. Animal Behaviour 2014, 97:313-321.
76. Roberts S.A., Davidson A.J., McLean L., Beynon R.J., Hurst J.L. Pheromonal induction of spatial learning in mice. Science 2012, 338:1462-1465.
77. Roberts S.A., Simpson D.M., Armstrong S.D., Davidson A.J., Robertson D.H., McLean L., et al. Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biology 2010, 8:75.
78. Robertson D.H.L., Marie A.D., Veggerby C., Hurst J.L., Beynon R.J. Characteristics of ligand binding and release by major urinary proteins. Chemical signals in vertebrates 9 2001, 169-176. Kluwer Academic/Plenum Publishers, Dordrecht, The Netherlands. A. Marchlewska-Koj, J.J. Lepri, D. Müller-Schwarze (Eds.).
79. Serrano R., Barata E., Birkett M., Hubbard P., Guerreiro P., Canário A. Behavioral and olfactory responses of female Salaria pavo (Pisces: Blenniidae) to a putative multi-component male pheromone. Journal of Chemical Ecology 2008, 34:647-658.
80. Setchell J.M., Huchard E. The hidden benefits of sex: evidence for MHC-associated mate choice in primate societies. Bioessays 2010, 32:940-948.
81. Smadja C., Butlin R.K. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 2009, 102:77-97.
82. Snell T.W. Contact chemoreception and its role in zooplankton mate recognition. Chemical communication in crustaceans 2011, 451-466. Springer, New York, NY. T. Breithaupt, M. Thiel (Eds.).
83. Thomas M.L., Simmons L.W. Crickets detect the genetic similarity of mating partners via cuticular hydrocarbons. Journal of Evolutionary Biology 2011, 24:1793-1800.
84. Touhara K. Sexual communication via peptide and protein pheromones. Current Opinion in Pharmacology 2008, 8:759-764.
85. Toyoda F., Yamamoto K., Iwata T., Hasunuma I., Cardinali M., Mosconi G., et al. Peptide pheromones in newts. Peptides 2004, 25:1531-1536.
86. Wabnitz P.A., Bowie J.H., Tyler M.J., Wallace J.C., Smith B.P. Aquatic sex pheromone from a male tree frog. Nature 1999, 401:444-445.
87. Wilkins M.R., Sanchez J.-C., Gooley A.A., Appel R.D., Humphery-Smith I., Hochstrasser D.F., et al. Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnology and genetic engineering reviews 1996, 13:19-50.
88. Wolfner M.F. Battle and ballet: molecular interactions between the sexes in Drosophila. Journal of Heredity 2009, 100:399-410.
89. Woodley S.K. Pheromonal communication in amphibians. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 2010, 196:713-727.
90. Woodley S.K. Chemical signaling in amphibians. Neurobiology of chemical communication 2014, 255-284. CRC Press, Boca Raton, FL. C. Mucignat-Caretta (Ed.).
91. Wyatt T.D. Fifty years of pheromones. Nature 2009, 457:262-263.
92. Wyatt T.D. 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 2010, 196:685-700.
93. Wyatt T.D. Pheromones and animal behavior: Chemical signals and signatures 2014, Cambridge University Press, Cambridge, U.K. 2nd ed.
94. Yamazaki K., Beauchamp G.K. Genetic basis for MHC-dependent mate choice. Advances in genetics 2007, 59:129-145.
95. Yambe H., Kitamura S., Kamio M., Yamada M., Matsunaga S., Fusetani N., et al. l-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:15370-15374.
96. Yang C.H., Rumpf S., Xiang Y., Gordon M.D., Song W., Jan L.Y., et al. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 2009, 61:519-526.
97. Yoshinaga S., Sato T., Hirakane M., Esaki K., Hamaguchi T., Haga-Yamanaka S., et al. Structure of the mouse sex peptide pheromone ESP1 reveals a molecular basis for specific binding to the class C G-protein-coupled vomeronasal receptor. Journal of Biological Chemistry 2013, 288:16064-16072.
98. Ziegler T.A., Forward R.B. Larval release behaviors in the Caribbean spiny lobster, Panulirus argus: role of peptide pheromones. Journal of Chemical Ecology 2007, 33:1795-1805.
99. Zimmer-Faust R.K., Tamburri M.N. Chemical identity and ecological implications of a waterborne, larval settlement cue. Limnology and Oceanography 1994, 39:1075-1087.
100. van Zweden J.S., d'Ettorre P. Nestmate recognition in social insects and the role of hydrocarbons. Insect hydrocarbons: Biology, biochemistry, and chemical ecology 2010, 222-243. Cambridge University Press, Cambridge, U.K. G.J. Blomquist, A.-G. Bagnères (Eds.).