Fishy aroma of social status: urinary chemo-signalling of territoriality in male fathead minnows (Pimephales promelas).

Dalma Martinovic-Weigelt, Drew R Ekman, Daniel L Villeneuve, Channing M James, Quincy Teng, Timothy W Collette, Gerald T Ankley
Author Information
  1. Dalma Martinovic-Weigelt: Department of Biology, University of St. Thomas, St. Paul, Minnesota, United States of America. dalma@stthomas.edu

Abstract

Chemical structures of several urinary reproductive pheromones in fish have been identified, and their role in the chemical communication of reproductive condition is well characterized. On the contrary, the role of chemical communication in signalling of social/territorial status in fish is poorly understood. Fathead minnows are an example of a fish species whose life history traits appear conducive to evolution of chemical communication systems that confer information about social/territorial status. Male reproduction in this species is dependent upon their ability to acquire and defend a high quality nesting territory, and to attract a female to the nest. We hypothesized that fathead minnow males use visual and urine-derived chemical cues to signal territorial status. To test this hypothesis, effects of territorial acquisition on male-specific secondary sex characteristics (SSCs) and urine volumes were first assessed. Second, frequencies of male urination in varying social contexts were examined. Finally, nuclear magnetic resonance-based metabolomics was used to identify urinary metabolites that were differentially excreted in the urine of territorial versus non-territorial males. The expression of SSCs, sperm, and urine volumes increased with territory acquisition, and either remained unchanged or decreased in non-territorial males. Frequency of male urination increased significantly in the presence of females (but not males), suggesting that females are the main target of the urinary signals. Territorial and non-territorial males had distinct urinary metabolomic profiles. An unforeseen finding was that one could discern future territorial status of males, based on their initial metabolomic profiles. Bile acids and volatile amines were identified as potential chemical signals of social status in the fathead minnow. The finding that trimethylamine (a fishy smelling volatile amine) may be a social cue is particularly interesting, because it is known to bind trace amine-associated receptors, indicating that these receptors may play role in chemical signalling of social status in fish.

References

  1. Amino Acids. 2012 Aug;43(2):773-81 [PMID: 22045384]
  2. Horm Behav. 2010 Jul;58(2):230-40 [PMID: 20303357]
  3. J Exp Biol. 2012 Jan 1;215(Pt 1):68-74 [PMID: 22162854]
  4. Am Nat. 2002 Dec;160 Suppl 6:S186-97 [PMID: 18707476]
  5. J Chem Ecol. 2004 Nov;30(11):2091-110 [PMID: 15672658]
  6. Comp Biochem Physiol C Toxicol Pharmacol. 2001 Dec;130(4):467-76 [PMID: 11738634]
  7. Pharmacol Biochem Behav. 2007 Jun-Jul;87(2):222-31 [PMID: 17553555]
  8. Horm Behav. 2004 Apr;45(4):235-41 [PMID: 15053939]
  9. J Exp Biol. 2010 Jan 15;213(2):308-17 [PMID: 20038666]
  10. Science. 2002 Apr 5;296(5565):138-41 [PMID: 11935026]
  11. Can J Zool. 1974 Aug;52(8):1031-8 [PMID: 4418744]
  12. J Exp Biol. 2009 Aug;212(Pt 15):2464-74 [PMID: 19617440]
  13. Physiol Biochem Zool. 2006 Jul-Aug;79(4):675-87 [PMID: 16826494]
  14. Ann N Y Acad Sci. 2009 Jul;1170:168-72 [PMID: 19686131]
  15. Acta Physiol Scand. 1980 Feb;108(2):123-31 [PMID: 7376910]
  16. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14171-6 [PMID: 10570217]
  17. Chem Senses. 2005 Jan;30 Suppl 1:i309-10 [PMID: 15738173]
  18. Trends Ecol Evol. 2001 Apr 1;16(4):184-190 [PMID: 11245941]
  19. J Chem Ecol. 2008 Apr;34(4):438-49 [PMID: 18379847]
  20. J Chem Ecol. 2005 Aug;31(8):1845-64 [PMID: 16222811]
  21. J Exp Biol. 2008 Sep;211(Pt 18):3041-56 [PMID: 18775941]
  22. Proc Biol Sci. 2004 Jan 7;271(1534):7-13 [PMID: 15002765]
  23. Nature. 2006 Aug 10;442(7103):645-50 [PMID: 16878137]
  24. J Chem Ecol. 1992 Jul;18(7):1269-84 [PMID: 24254164]
  25. J Theor Biol. 1974 Sep;47(1):223-43 [PMID: 4477626]
  26. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2009 Jul;195(7):691-8 [PMID: 19415298]
  27. Proc Biol Sci. 2008 Oct 22;275(1649):2393-402 [PMID: 18628117]
  28. Comp Biochem Physiol B Biochem Mol Biol. 2002 May;132(1):203-15 [PMID: 11997222]
  29. Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4313-8 [PMID: 19237578]
  30. J Comp Physiol B. 2001 Mar;171(2):161-71 [PMID: 11302533]
  31. J Exp Biol. 2001 Nov;204(Pt 22):3867-76 [PMID: 11807104]
  32. PLoS One. 2008;3(12):e4083 [PMID: 19116654]
  33. Horm Behav. 2004 Jun;46(1):11-8 [PMID: 15215037]
  34. Environ Toxicol Chem. 2007 Feb;26(2):271-8 [PMID: 17713215]
  35. Behav Processes. 2009 Nov;82(3):279-85 [PMID: 19635532]
  36. Environ Sci Technol. 2010 Sep 1;44(17):6881-6 [PMID: 20687545]
  37. BMC Biol. 2007 Dec 12;5:54 [PMID: 18076759]
  38. Neurosci Biobehav Rev. 2005;29(8):1123-44 [PMID: 16085312]
  39. Physiol Behav. 1999 Jan 1-15;65(4-5):665-9 [PMID: 10073465]
  40. J Chem Ecol. 2008 Jul;34(7):898-914 [PMID: 18521679]
  41. Gen Comp Endocrinol. 2006 Oct;149(1):30-41 [PMID: 16765351]
  42. Aquat Toxicol. 2007 Nov 30;85(2):104-12 [PMID: 17897733]
  43. Pharmacol Biochem Behav. 2006 Feb;83(2):271-6 [PMID: 16540157]

MeSH Term

Animals
Cyprinidae
Female
Male
Metabolome
Sexual Behavior, Animal
Territoriality
Urination
Urine

Word Cloud

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