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Chemical and behavioural characterization of the rabbit mammary pheromone

Abstract

Mammals owe part of their evolutionary success to the harmonious exchanges of information, energy and immunity between females and their offspring. This functional reciprocity is vital for the survival and normal development of infants, and for the inclusive fitness of parents1,2. It is best seen in the intense exchanges taking place around the mother's offering of, and the infant's quest for, milk. All mammalian females have evolved behavioural and sensory methods of stimulating and guiding their inexperienced newborns to their mammae, whereas newborns have coevolved means to respond to them efficiently3. Among these cues, maternal odours have repeatedly been shown to be involved4,5,6, but the chemical identity and pheromonal nature of these cues have not been definitively characterized until now. Here we focus on the nature of an odour signal emitted by the female rabbit to which newborn pups respond by attraction and oral grasping, and provide a complete chemical and behavioural description of a pheromone of mammary origin in a mammalian species.

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Figure 1: The GCO assay.
Figure 2: Screening, by the glass-rod assay, of milk volatiles presumed to have behavioural activity.
Figure 3: The key impact of 2MB2 in milk (glass-rod assays; open bars and squares, searching; solid bars and squares, grasping).
Figure 4: Selectivity, specificity and independence from learning of pup responsiveness to 2MB2 (glass-rod assays; open bars, searching; solid bars, grasping).

References

  1. Clutton-Brock, T. H. The Evolution of Parental Care (Princeton Univ. Press, 1991)

    Google Scholar 

  2. Rosenblatt, J. S. & Snowdon, T. C. Parental Care, Evolution, Mechanisms and Adaptive Significance (Academic, Orlando, 1996)

    Google Scholar 

  3. Rosenblatt, J. S. Olfaction mediates developmental transition in the altricial newborn of selected species of mammals. Dev. Psychobiol. 16, 347–375 (1983)

    CAS  Article  Google Scholar 

  4. Leon, M. & Moltz, H. Maternal pheromone: Discrimination by pre-weanling albino rats. Physiol. Behav. 7, 265–267 (1971)

    CAS  Article  Google Scholar 

  5. Blass, E. M. & Teicher, M. H. Suckling. Science 210, 15–22 (1980)

    ADS  CAS  Article  Google Scholar 

  6. Macfarlane, A. J. Olfaction in the development of social preferences in the human neonate. Ciba Found. Symp. 33, 103–117 (1975)

    Google Scholar 

  7. Zarrow, M. X., Denenberg, V. H. & Anderson, C. O. Rabbit: Frequency of suckling in the pup. Science 150, 1835–1836 (1965)

    ADS  CAS  Article  Google Scholar 

  8. Coureaud, G. et al. Immediate postnatal sucking in the rabbit: Its influence on pup survival and growth. Reprod. Nutr. Dev. 40, 19–32 (2000)

    CAS  Article  Google Scholar 

  9. Schley, P. Geruchssinn und Saugverhalten bei Jungkaninchen. Kleintier Praxis 26, 261–263 (1981)

    Google Scholar 

  10. Hudson, R. & Distel, H. Nipple location by newborn rabbits: Evidence for pheromonal guidance. Behaviour 85, 260–275 (1983)

    Article  Google Scholar 

  11. Coureaud, G. & Schaal, B. Attraction of newborn rabbits to abdominal odors of adult conspecifics differing in sex and physiological state. Dev. Psychobiol. 36, 271–281 (2000)

    CAS  Article  Google Scholar 

  12. Keil, W., von Stralendorff, F. & Hudson, R. A behavioral bioassay for analysis of rabbit nipple-search pheromone. Physiol. Behav. 47, 525–529 (1990)

    CAS  Article  Google Scholar 

  13. Coureaud, G., Schaal, B., Langlois, D. & Perrier, G. Orientation response of newborn rabbits to odours of lactating females: Relative effectiveness of surface and milk cues. Anim. Behav. 61, 153–162 (2001)

    Article  Google Scholar 

  14. Coureaud, G. Régulation Olfactive de la Prise Lactée chez le Lapereau: Caractérisation Éthologique et Chimique d'un Signal Phéromonal. Thesis, Univ. Paris 13 (2001)

    Google Scholar 

  15. Beauchamp, G. K., Doty, R. L., Moulton, D. G. & Mugford, R. A. in Olfaction, Behavior, and Mammalian Reproduction (ed. Doty, R. L.) 143–160 (Academic, New York, 1976)

    Book  Google Scholar 

  16. Johnston, R. E. in The Neurobiology of Taste and Smell, 2nd edn (eds Finger, T. E., Silver, W. L. & Restrepo, D.) 101–127 (Wiley-Liss, New York, 2000)

    Google Scholar 

  17. Goodrich, B. S., Hesterman, E. R., Shaw, K. S. & Mykytowycz, R. Identification of some volatile compounds in the odor of fecal pellets of the rabbit, Oryctolagus cuniculus. J. Chem. Ecol. 7, 817–827 (1981)

    CAS  Article  Google Scholar 

  18. Pedersen, P. A. & Blass, E. M. in The Development of Perception: Psychobiological Perspectives (eds Aslin, R. N., Alberts, J. R. & Petersen, M. R.) 359–381 (Academic, New York, 1981)

    Book  Google Scholar 

  19. Galef, B. G., Mason, J. F., Preti, G. & Bean, N. J. Carbon disulfide: A semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42, 119–124 (1988)

    CAS  Article  Google Scholar 

  20. Coureaud, G., Schaal, B., Hudson, R., Orgeur, P. & Coudert, P. Transnatal olfactory continuity in the rabbit: Behavioral evidence and short-term consequence of its disruption. Dev. Psychobiol. 40, 372–390 (2002)

    Article  Google Scholar 

  21. Muller-Schwarze, D. et al. in Chemical Signals in Vertebrates 4 (eds Duvall, D., Muller-Schwarze, D. & Silverstein, R. M.) 561–570 (Plenum, New York, 1986)

    Book  Google Scholar 

  22. Morrow-Tesch, J. & McGlone, J. J. Sensory systems and nipple attachment behavior in neonatal pigs. Physiol. Behav. 47, 1–4 (1989)

    Article  Google Scholar 

  23. Teicher, M. H. & Blass, E. M. First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science 198, 635–636 (1977)

    ADS  CAS  Article  Google Scholar 

  24. Sam, M. et al. Odorants may arouse instinctive behaviours. Nature 412, 142 (2001)

    ADS  CAS  Article  Google Scholar 

  25. Zou, Z., Horowitz, L. F., Montmayeur, J. P., Snapper, S. & Buck, L. B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173–179 (2001)

    ADS  CAS  Article  Google Scholar 

  26. Johnson, B. A. & Leon, M. Odorant molecular length: One aspect of the olfactory code. J. Comp. Neurol. 426, 330–338 (2000)

    CAS  Article  Google Scholar 

  27. Uchida, N., Takahashi, Y., Tanifuji, M. & Mori, K. Odor maps in the mammalian olfactory bulb: Domain organization and odorant structural features. Nature Neurosci. 3, 1035–1043 (2000)

    CAS  Article  Google Scholar 

  28. Abbott, N., Etievant, P., Issanchou, S. & Langlois, D. Critical evaluation of two commonly used techniques for the treatment of data from extract dilution sniffing analysis. J. Agric. Food Chem. 41, 1698–1703 (1993)

    CAS  Article  Google Scholar 

  29. Schley, P. Untersuchung zur kuenstlichen Aufzucht von Hauskaninchen. Thesis, Univ. Giessen (1976)

    Google Scholar 

  30. Lebas, F. Description d'une machine à traire les lapines. Ann. Zootech. 19, 223–228 (1970)

    Article  Google Scholar 

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Acknowledgements

We thank J. L. Le Quéré for support and advice; P. Coudert, J. Ponceau, J. L. Vrillon and P. Mercier for giving access to their colonies; P. Orgeur, J. P. Drouet, M. Jouanno, F. Lebas, L. Fortun-Lamothe, M. Theau-Clément, G. Thébault, G. Bolet, A. Locatelli, Y. Breuzin and J. P. Francinot for contributions; D. Licois and R. Hudson for providing Lebas' and Schley's milking devices; R. L. Doty, V. H. Dennenberg, A. Holley, J. P. Montmayeur, P. Coudert, R. Hudson, P. Salin and H. Distel for discussions; and R. Langlois, E. Hertling and C. Ferdenzi for logistic support. This work was conducted in part while B.S. and G.C. were at Unité de Physiologie de la Reproduction, CNRS-Inra, Nouzilly, France. G.C. was sponsored by Région Poitou-Charente-Inra and the Fyssen Foundation.

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Correspondence to Benoist Schaal.

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Schaal, B., Coureaud, G., Langlois, D. et al. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424, 68–72 (2003). https://doi.org/10.1038/nature01739

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