PhD, Florida State University
Structure, function, metabolism and molecular evolution of salamander courtship pheromones
Drs. Rick and Pam Feldhoff have a productive collaboration with Drs. Lynne Houck and Stevan Arnold at Oregon State University on the effects of courtship pheromones on reproductive behavior in Plethodontid salamanders. During courtship, a male Plethodon shermani salamander delivers pheromones from a submandibular mental gland to the female’s nares. Following binding of pheromones to receptors in the vomeronasal organ, areas of the brain associated with sexual behavior are stimulated and female receptivity increases. The pheromone mixture consists of two major families, each of which contains multiple isoforms. The 22 kDa family (Plethodontid Receptivity Factor; PRF) is related to the IL-6 family of cytokines, while the 7 kDa family (Plethodontid Modulating Factor; PMF) is related to xenoxins and snake cytotoxins. Efforts at Oregon State focus on the behavioral biology aspects of the project. Current research efforts in our lab, utilizing contemporary techniques in protein biochemistry, molecular biology, mass spectral analyses, proteomics and 2D-NMR are focused on the purification and structural characterization of the PRF and PMF isoforms, including the determination of the complex disulfide bonding pattern for PMF and its 3-dimensional structure. Recently, we have begun to focus on: gene structure and transcriptional and translational regulation in the mental gland; and, histological and immunohistochemical analyses of the vomeronasal organ and the mental gland. Pheromone studies are also being extended to the more primitive species, Desmognathus ocoee and Plethodon cinereus both of which use a more complex pheromone mixture and a different mode of pheromone delivery.
Wilburn DB, Bowen KE, Gregg RG, Cai J, Feldhoff PW, Houck LD and Feldhoff RC (2012). Proteomic and UTR analyses of a rapidly evolving hypervariable family of vertebrate pheromones. Evolution 66(7):2227-2239. doi:10.1111/j.1558-5646.2011.01572.x Epub 2012 Feb 17. PMID: 22759298
Chouinard, A.J., Wilburn, D.B., Houck, L.D. and Feldhoff, R.C. (2012). Individual variation in pheromone isoform ratios of the red-legged salamander, Plethodon shermani. In: East ML,Dehnhard M (eds.) Chemical Signals in Vertebrates 12. Springer Verlag, Berlin, Germany (in press).
Wack, C.L., DuRant, S.E., Hopkins, W.A., Lovern, M.B., Feldhoff, R.C. and Woodley, S.K. (2012). Elevated plasma corticosterone increases metabolic rate in a terrestrial salamander. Comp Biochem Physiol A Mol Integr Physiol. 161(2):153-8. Epub 2011 Oct 25. PMID: 22047668
Kiemnec-Tyburczy, K.M., Woodley, S.K., Feldhoff, P.W., Feldhoff, R.C. and Houck, L.D. (2011). Dermal application of courtship pheromones does not influence receptivity in female red-legged salamanders (Plethodon shermani). J. Herpetology 45(2):169-173. doi: 10.1670/10-014.1
Vaccaro, E.A., Feldhoff, P.W., Feldhoff, R.C. and Houck L.D. (2010). A pheromone mechanism for swaying female mate choice: enhanced affinity for a sexual stimulus in a woodland salamander. Animal Behaviour 80: 983-989.
Vaccaro, E.A., Feldhoff, P.W., Feldhoff, R.C. and Houck L.D. (2009). Male courtship pheromones suppress female tendency to feed but not to flee in a plethodontid salamander. Animal Behaviour 78: 1421-1425.
Schubert SN, Wack CL, Houck LD, Feldhoff PW, Feldhoff RC, and Woodley SK. (2009) Exposure to pheromones increases plasma corticosterone concentrations in a terrestrial salamander. Gen Comp Endocrinol. 2009 Apr;161(2):271-5. Epub 2009 Jan 31. PMID: 19523389
Houck LD, Watts RA, Arnold SJ, Bowen KE, Kiemnec KM, Godwin HA, Feldhoff PW, and Feldhoff RC. (2008) A recombinant courtship pheromone affects sexual receptivity in a plethodontid salamander. Chem. Senses 33:623-631. Epub 2008 Jun 5. PMID: 18534996.
Schubert SN, Houck LD, Feldhoff PW, Feldhoff RC and Woodley SK. (2008) The effects of sex and female reproductive condition on chemosensory communication in a terrestrial salamander (Plethodon shermani). Hormones and Behavior 54:270-277.
Laberge F, Feldhoff RC, Feldhoff PW, Houck LD. (2008) Courtship pheromone-induced c-Fos-like immunolabeling in the female salamander brain. Neuroscience.151(2):329-39. Epub 2007 Nov 17. PMID: 18082970
Houck LD, Watts RA, Mead LM, Palmer CA, Arnold SJ, Feldhoff PW and Feldhoff RC. (2007) A candidate vertebrate pheromone, SPF, increases female receptivity in a salamander. pp 213-221. In: J. Hurst, R. Beynon, and D. Muller-Schwarze, (eds.), Chemical Signals in Vertebrates 11, Springer, New York.
Palmer CA, Hollis DM, Watts RA, Houck LD, McCall MA, Gregg RG, Feldhoff PW, Feldhoff RC and Arnold SJ. (2007) Plethodontid Modulating Factor (PMF), a hyper-variable salamander courtship pheromone in the three-finger protein superfamily. FEBS Journal 274(9):2300-2310.
Houck LD, Palmer CA, Watts RA, Arnold SJ, Feldhoff PW and Feldhoff RC. (2007) A new vertebrate courtship pheromone, PMF, affects female receptivity in a terrestrial salamander. Animal Behaviour 73: 315-320.
Schubert SN, Houck LD, Feldhoff PW, Feldhoff RC and Woodley SK. (2006). Effects of androgens on behavioral and vomeronasal responses to chemosensory cues in male terrestrial salamanders (Plethodon shermani). Hormones and Behavior 50 (3):469-476. PMID: 16860800.
Wirsig-Wiechmann CR, Houck LD, Wood JM, Feldhoff PW and Feldhoff RC. (2006) Male pheromone protein components activate female vomeronasal neurons in the salamander Plethodon shermani. BMC Neuroscience 7:26. PMID: 16553953
Stapp JM, Sjoelund V, Lassiter HA, Feldhoff RC and Feldhoff PW. (2005) Recombinant rat IL-1-beta and IL-6 synergistically enhance C3 mRNA levels and complement component C3 secretion. Cytokine 30 (2): 78-85.
Watts RA, Palmer CA, Feldhoff RC, Feldhoff PW, Houck LD, Jones AG, Pfrender ME, Rollmann SM and Arnold SJ (2004) Stabilizing selection on behavior and morphology masks positive selection on the signal in a salamander pheromone signaling complex. Molecular Biology and Evolution 21 (6): 1032-1041.
Rollmann SM, Houck LD, and Feldhoff RC. (2003) Conspecific and heterospecific pheromone effects on female receptivity. Animal Behaviour 66, 857-861.
Andrews, E., Feldhoff, P, Feldhoff, R and Lassiter, H. (2003) Comparative effects of cytokines and cytokine combinations on complement component C3 secretion by HepG2 cells. Cytokine 23: 164-169.
Wirsig-Wiechmann CR, Houck LD, Feldhoff PW and Feldhoff RC. (2002) Pheromonal activation of vomeronasal neurons in plethodontid salamanders. Brain Research 952(2): 335-344.
Rollmann SM, Houck LD, and Feldhoff RC. (2000) Population variation in salamander courtship pheromones. J. Chem. Ecol. 26, 2713-2723.
Rollmann SM, Houck LD, and Feldhoff RC. (1999) Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science 285, 1907-1909.
Feldhoff, R.C., Rollmann, S.M., and Houck, L.D. (1999) Chemical analysis of courtship pheromones in a plethodontid salamander. In: Advances in Chemical Signals in Vertebrates; pp 117-125; R. E. Johnston, D. Müller-Schwarze and P. Sorensen (Eds.). Kluwer Academic/Plenum Publishers, New York.