Journal of Chemical Ecology

, Volume 35, Issue 5, pp 580–589 | Cite as

Comparison of Urinary Scents of Two Related Mouse Species, Mus spicilegus and Mus domesticus

  • Helena A. Soini
  • Donald Wiesler
  • Sachiko Koyama
  • Christophe Féron
  • Claude Baudoin
  • Milos V. Novotny


Whereas the house mouse (Mus domesticus) has been studied extensively in terms of physiology/behavior and pheromonal attributes, the evolutionarily related mound-building mouse (Mus spicilegus) has received attention only recently due to its divergent behavioral traits related to olfaction. To date, no chemical studies on urinary volatile compounds have been performed on M. spicilegus. The rationale for our investigations was to determine if there are differences in urinary volatiles of intact and castrated M. spicilegus males and to explore further whether this species could utilize the same or structurally similar pheromones as the male house mouse, M. domesticus. The use of capillary gas chromatography/mass spectrometry (GC-MS) together with sorptive stir bar extraction sampling enabled quantitative comparisons between the intact and castrated M. spicilegus urinary profiles. Additionally, through GC-MS and atomic emission (sulfur-selective) detection, we identified qualitative molecular differences between intact M. spicilegus and M. domesticus. A series of volatile and odoriferous lactones and the presence of coumarin were the unique features of M. spicilegus, as was the notable absence of 2-sec-butyl-4,5-dihydrothiazole (a prominent M. domesticus male pheromone) and other sulfur-containing compounds. Castration of M. spicilegus males eliminated several substances, including δ-hexalactone and γ-octalactone, and substantially decreased additional compounds, suggesting their possible role in chemical communication. Some other M. domesticus pheromone components were also found in M. spicilegus urine. These comparative chemical analyses support the notion of metabolic similarities as well as the uniqueness of some volatiles for M. spicilegus, which may have a distinct physiological function in reproduction and behavior.


Mus spicilegus Mus domesticus Urinary volatile profile Gas chromatography/mass spectrometry Stir bar extraction Pheromones 


  1. Albrecht, W., Heidlas, J., Schwarz, M., and Tressl, R. 1992. Biosynthesis and biotechnological production of aliphatic γ- and δ-lactones, pp. 45-58, in T. Teranishi, G.R. Takeoka, and M. Güntert (eds.). Flavor Precursors, Thermal and Enzymatic Conversions , ACS Symposium Series 490, American Chemical Society, Washington.Google Scholar
  2. Baudoin, C., Busquet, N., Dobson, F.S., Gheusi, G., Féron, C., Durand, J.L., Heth, G., Patris, B., and Todrank, J. 2005. Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus. Biol. J. Linnean Soc. 84:323-334.CrossRefGoogle Scholar
  3. Baltussen, E., Sandra, P., David, F., and Cramers, C.A. 1999. Stir bar sorptive extraction (SBSE), a novel extraction technique for aqueous sample: Theory and principles. J. Microcol. Separations 11:737-747.CrossRefGoogle Scholar
  4. Baltussen, E., Cramers, C.A., and Sandra, P.J.F. 2002. Sorptive sample preparation – a review. Anal. Bioanal. Chem. 373:2-22.Google Scholar
  5. Blum, M.S., Fales, H.M., Morse, R.A., and Underwood, B.A. 2000. Chemical characters of two related species of giant honeybees (Apis dorsata and A. laboriosa): possible ecological significance. J. Chem. Ecol. 26:801-807.CrossRefGoogle Scholar
  6. Bonhomme, F., Catalan, J., Britton-Davidian, J., Chapman, V.M., Moriwaki, K., Nevo, E., and Thaler, L. 1984. Biochemical diversity and evolution in the genus Mus. Biochem. Genetics 22:275-303.CrossRefGoogle Scholar
  7. Bourgaud, F., Hehn, A., Larbat, R., Doerper, S., Gontier, E., Kellner, S., and Matern, U. 2006. Biosynthesis of coumarins in plants: a major pathway still to be unraveled for cytochrome P450 enzymes. Phytochem. Rev. 5:293-308.CrossRefGoogle Scholar
  8. Boyer, M.L., Jemiolo, B., Andreolini, F., Wiesler, D., and Novotny, M. 1989. Urinary volatile profiles of pine vole, Microtus pinetorum, and their endocrine dependency. J. Chem. Ecol. 15:649-662.CrossRefGoogle Scholar
  9. Brown, R.E. 1985. The rodent II: suborder Myomorpha, pp. 345-457, in R. E Brown and D.W. Macdonald (eds.). Social Odours in Mammals, Vol 1, Clarendon, Oxford.Google Scholar
  10. Busquet, N., and Baudoin, C. 2005. Odour similarities as a basis for discriminating degrees of kinship in rodents: evidence from Mus spicilegus. Anim. Behav. 70:997-1002.CrossRefGoogle Scholar
  11. Colombelli-NEGREL, D., and Gouat, P. 2006. Male and female mound-building mice, Mus spicilegus, discriminate dietary and individual odours of conspecifics. Anim. Behav. 72:577-583.CrossRefGoogle Scholar
  12. Creaven, P.J., Parke, D.V., and Williams, R.T. 1965. A spectrofluorimetric study of the 7-hydroxylation of coumarin by liver microsomes. Biochem. J. 96:390-398.PubMedGoogle Scholar
  13. Dickschat, J.S., Wagner-Döbler, I., and Schulz, S. 2005. The chafer pheromone buibuilactone and ant pyrazines are also produced by marine bacteria. J. Chem. Ecol. 31:925-947.PubMedCrossRefGoogle Scholar
  14. Dobson, F.S., and Baudoin, C. 2002. Experimental tests of spatial association and kinship in monogamous mice (Mus spicilegus) and polygynous mice (Mus musculus domesticus). Canadian J. Zool. 80:980-986.CrossRefGoogle Scholar
  15. Féron, C., and Baudoin, C. 1993. Sexual experience and preferences for odors of estrous females in staggerer mutant mice. Behav. Neurol. Biol. 60:280-281.CrossRefGoogle Scholar
  16. Féron, C., and Baudoin, C. 1998. Social isolation induces preference for odours of oestrous females in sexually naïve male staggerer mutant mice. Chem. Senses, 23:119-121.PubMedCrossRefGoogle Scholar
  17. Féron, C., and Gheusi, G. 2003. Social regulation of reproduction in the female mound-builder mouse (Mus spicilegus). Physiol. Behav. 78:717-722.PubMedCrossRefGoogle Scholar
  18. Féron, C., and Gouat, P. 2007. Paternal care in the mound-building mouse reduces inter-litter intervals. Reprod. Fertility Devel. 19:425-429.CrossRefGoogle Scholar
  19. Garza, J.C., Dallas, J., Duryadi, D., Gerasimov, S., Croset, H., and Boursot, P. 1997. Social structure of the mound-building mouse Mus spicilegus revealed by genetic analysis with microsatellites. Molecular Ecol. 6:1009-1017.CrossRefGoogle Scholar
  20. Gatfield, I.L., Güntert, M., Sommer, H., and Werkhoff, P. 1993. Some aspects of the microbial production of flavor-active lactones with particular reference to γ-decalactone. Chem., Mikrobiol. Technol. Lebensmittel 15:165-170.Google Scholar
  21. Gouat, P., Patris, B., and Lalande, C. 1998. Conspecific and heterospecific behavioural discrimination of individual odours by mound-building mice. Comptes Rendus de l’Académie des Sciences Paris, Sciences de la vie 321:571-575.PubMedGoogle Scholar
  22. Gouat, P. and Féron, C. 2005. Deficit in reproduction in polygynously mated females of the monogamous mound-building mouse Mus spicilegus. Reprod. Fertility Devel. 17: 617-623.CrossRefGoogle Scholar
  23. Haffner, T., and Tressl, R. 1996. Biosynthesis of (R)-γ-decanolactone in the yeast Sporobolomyces odorus. J. Agric. Food Chem. 44:1218-1223.CrossRefGoogle Scholar
  24. Harvey, S., Jemiolo, B., and Novotny, M. 1989. Pattern of volatile compounds in dominant and subordinate male mouse urine. J. Chem. Ecol. 15:2061-2072.CrossRefGoogle Scholar
  25. Heth, G., Todrank, J., Busquet, N., and Baudoin, C. 2001. Odour-genes covariance and differential investigation of individual odours in the Mus species complex. Biol. J. Linnean Soc.73:213-220CrossRefGoogle Scholar
  26. Heth, G., Todrank, J., Busquet, N., and Baudoin C., 2003. Genetic relatedness assessment through individual odour similarities in mice. Biol. J. Linnean Soc. 78:595-603.CrossRefGoogle Scholar
  27. Hurst, J.L., and Beynon, R.J. 2004. Scent wars: the chemobiology of competitive signaling in mice. BioEssays 26:1288-1298.PubMedCrossRefGoogle Scholar
  28. Jemiolo, B., Xie, T.M., Andreolini, F., Baker, A.E.M., and Novotny, M. 1991. The t complex of the mouse: chemical characterization by urinary volatile profiles. J. Chem. Ecol. 17:353-367.CrossRefGoogle Scholar
  29. Juvonen, R.O., Iwasaki, M., and Negishi, M. 1991. Structural function of residue-209 in coumarin 7-hydroxylase (P450coh). J. Biol. Chem. 266:16431-16435.PubMedGoogle Scholar
  30. Juvonen, R.O., Gynther, J., Pasanen, M., Alhava, E., and Poso, A. 2000. Pronounced differences in inhibition potency of lactone and non-lactone compounds for mouse and human coumarin 7-hydroxylases (CYP2A5 and CYP2A6). Xenobiotica 30:81-92.PubMedCrossRefGoogle Scholar
  31. Kimoto, H., Haga, S., Sato, K., and Touhara, K. 2005. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901.PubMedCrossRefGoogle Scholar
  32. Laukaitis, C.M, Crister, E.S., and Karn, R.C. 1997. Salivary androgen-binding protein (ABP) mediates assortative mate selection in Mus musculus. Evolution 51:2000-2005.CrossRefGoogle Scholar
  33. Lewis, D.F.V., and Lake, B.G. 2002. Species differences in coumarin metabolism: a molecular modeling evaluation of CYP2A interactions. Xenobiotica 32:547-561.PubMedCrossRefGoogle Scholar
  34. Miles, J.S., Mclare, A.W., Forrester, L.M., Glancey, M.J., Lang, M.A., and Wolf, C.R. 1990. Identification of the human liver cytochrome P-450 responsible for coumarin 7-hydroxylase activity. Biochem. J. 267:365-371.PubMedGoogle Scholar
  35. North, M., and Pattenden, G. 1990. Synthetic studies towards cyclic peptides. Concise synthesis of thiazoline and thiazole containing amino acids. Tetrahedron 46: 8267-8290.Google Scholar
  36. Novotny, M., Jorgenson, J.W., Carmack, M, Wilson, S.R., Boyse, E.A., Yamazaki, K., Wilson, M., Beamer, W., and Whitten, W.K. 1980. Chemical studies of the primer mouse pheromones, pp. 377-390, in D. Müller-Schwarze, and R.M .Silverstein (eds.). Chemical Signals in Vertebrates and Aquatic Invertebrates. Plenum, New York.Google Scholar
  37. Novotny, M. Harvey, S., Jemiolo, B., and Alberts, J. 1985. Syntheticpheromones that promote inter-male aggression in mice. Proc. Natl. Acad. Sci. USA 82:2059-2061.PubMedCrossRefGoogle Scholar
  38. Novotny, M., Harvey, S., and Jemiolo, B. 1990a. Chemistry of rodent pheromones: molecular insights into chemical signaling in mammals, pp.3-21, in D.W. McDonald, D. Müller-Schwarze, and S.E. Natynzuk (eds.). Chemical Signals in Vertebrates 5. Oxford University Press, Oxford.Google Scholar
  39. Novotny, M., Harvey, S., and Jemiolo, B. 1990b. Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109-113.PubMedCrossRefGoogle Scholar
  40. Novotny, M.V., Jemiolo, B., Wiesler, D., Ma, W., Harvey, S., Xu, F., Xie, T.M., and Carmack, M. 1999. A unique urinary constituent, 6-hydroxy-6-methyl-3-heptanone, has the puberty accelerating pheromone activity in mice. Chem. Biol. 6:377-383.PubMedCrossRefGoogle Scholar
  41. Novotny, M.V. 2003. Pheromones, binding proteins and receptor responses in rodents. Biochem. Soc. Transactions 31:117-122.CrossRefGoogle Scholar
  42. Novotny, M.V., Soini, H.A., Koyama, S., Bruce, K.E., Wiesler, D., Penn, D.J. 2007. Chemical identification of MHC-influenced volatile compounds in mouse urine. I: Quantitative proportions of major chemosignals. J. Chem. Ecol. 33:417-434.Google Scholar
  43. Orsini, P., Bonhomme, F., Britton-Davidian, J., Croset, H., Gerasimov, S., Thaler, L. 1983. Le complexe d’espèces du genre Mus en Europe Centrale et Orientale. II. Critères d’identification, répartition et caractéristiques écologiques. Zeitschr. für Säugetierk. 48:86–95Google Scholar
  44. Patris, B., and Baudoin, C. 1998. Female sexual preferences differ in Mus spicilegus and Mus musculus domesticus: the role of familiarization and sexual experience. Anim. Behav. 56:1465-1470.PubMedCrossRefGoogle Scholar
  45. Patris, B., and Baudoin, C. 2000. A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus. Behav. Proc. 51:35-43.CrossRefGoogle Scholar
  46. Patris, B., Gouat, P., Jacquot, C., Christophe, N., and Baudoin, C. 2002. Agonistic and sociable behaviors in the mound-building mice, Mus spicilegus: a comparative study with Mus musculus domesticus. Aggr. Behav., 28:75-84.CrossRefGoogle Scholar
  47. Poteaux, C., Busquet, N., Gouat, P., Katona, K., and Baudoin, C. 2008. Socio-genetic structure of mound-building mice, Mus spicilegus, in autumn and early spring. Biol. J. Linnean Soc., 93:689-699.CrossRefGoogle Scholar
  48. Ruddle, F.H., Shows, T.B., and Roderick, T.H. 1969. Esterase genetics in Mus musculus: expression, linkage, and polymorphism of locus Es-2. Genetics, 62:393-399.PubMedGoogle Scholar
  49. Sage, R.D., Atchley, W.R., and Capana, E. 1993. House mouse as models in systematic biology. System. Biol. 42:523-561.CrossRefGoogle Scholar
  50. Simeonovska-Nikolova, D.M. 2007. Spatial organization of the mound-building mouse Mus spicilegus in the region of northern Bulgaria. Acta Zool. Sinica 53:22-28.Google Scholar
  51. Soini, H.A., Bruce, K.E., Wiesler, D., David, F., Sandra, P., Novotny, M.V. 2005. Stir bar sorptive extraction: a new quantitative and comprehensive sampling technique for determination of chemical signal profiles from biological media. J. Chem. Ecol. 31:377-392.PubMedCrossRefGoogle Scholar
  52. Sokolov, V.E., Kotenkova, E.V., and Michailenko, A.G. 1998. Mus spicilegus. Mammalian Species 592:1-6.CrossRefGoogle Scholar
  53. Talley. H.M., Laukaitis, C.M., and Karn, R.C. 2001. Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies. Evolution 45:631-634.CrossRefGoogle Scholar
  54. Todrank, J., Busquet, N., Baudoin, C., and Heth, G. 2005. Preferences of newborn mice for odours indicating closer genetic relatedness: is experience necessary? Proc. Roy. Soc. London: Biol. Sci. 272:2083-2088.CrossRefGoogle Scholar
  55. Wiesler, D., Schwende, F.J., Carmack, M., and Novotny, M. 1984. Structural determination and synthesis of a chemical signal of the male state and potential multipurpose pheromone of the mouse, Mus musculus. J. Org. Chem. 49:882-884.CrossRefGoogle Scholar
  56. Wood, A.W. 1979. Genetic regulation of coumarin hydroxylase activity in mice. Biochemical characterization of the enzyme from two inbred strains and their F1 hybrid. J. Biol. Chem. 254:5641-5646.PubMedGoogle Scholar
  57. Wood, A.W., and Taylor, B.A. 1979. Genetic regulation of coumarin hydroxylase activity in mice. Evidence for single locus control on chromosome 7. J. Biol. Chem. 254:5647-5651.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Helena A. Soini
    • 1
  • Donald Wiesler
    • 1
  • Sachiko Koyama
    • 1
  • Christophe Féron
    • 2
  • Claude Baudoin
    • 2
  • Milos V. Novotny
    • 1
  1. 1.Department of Chemistry, Institute for Pheromone ResearchIndiana UniversityBloomingtonUSA
  2. 2.Laboratoire d’Ethologie Expérimentale et ComparéeUniversité Paris 13VilletaneuseFrance

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