Low temperature dormancy affects the quantity and quality of the female sexual attractiveness pheromone in red-sided garter snakes

Journal of Chemical Ecology

Volumn 35, Issue 10, 2009, Pages 1234-1241

  Parker, M Rockwell ^a   Mason, Robert T ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Attractivity; Gas chromatography mass spectrometry; Hibernation; Reproduction; Seasonality; Sex pheromone; Thamnophis sirtalis parietalis

Indexed keywords

LIPID; SEX PHEROMONE;

BIOCHEMISTRY; DEN; DORMANCY; GAS CHROMATOGRAPHY; HIBERNATION; LIPID; LOW TEMPERATURE; MASS SPECTROMETRY; OVERWINTERING; REPRODUCTIVE BEHAVIOR; SEX PHEROMONE; SNAKE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CHEMISTRY; COLD; FEMALE; HIBERNATION; MALE; PHYSIOLOGY; SEASON; SEXUAL BEHAVIOR; SKIN; SNAKE; TIME;

ANIMALS; COLD TEMPERATURE; COLUBRIDAE; FEMALE; HIBERNATION; LIPIDS; MALE; SEASONS; SEX ATTRACTANTS; SEXUAL BEHAVIOR, ANIMAL; SKIN; TIME FACTORS;

SERPENTES; THAMNOPHIS SIRTALIS PARIETALIS; VERTEBRATA;

EID: 76149142132     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-009-9699-0     Document Type: Article

References (65)

1. Aleksiuk, M. and Gregory, P. T. 1974. Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 1974: 681-689.
2. Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton.
3. Beach, F. A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav. 7: 105-138.
4. Bohnet, S., Rogers, L., Sasaki, G., and Kolattukudy, P. E. 1991. Estradiol induces proliferation of peroxisome-like microbodies and the production of 3-hydroxy fatty acid diesters, the female pheromones, in the uropygial glands of male and female mallards. J. Biol. Chem. 266: 9795-9804.
5. Bona-Gallo, A. and Licht, P. 1983. Effects of temperature on sexual receptivity and ovarian recrudescence in the garter snake Thamnophis sirtalis parietalis. Herpetol. 39: 173-182.
6. Bruce, H. M. 1965. Effect of castration on the reproductive pheromones of male mice. J. Reprod. Fertil. 10: 141-143.
7. Camazine, B., Garstka, W. R., Tokarz, R., and Crews, D. 1980. Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Horm. Behav. 14: 358-372.
8. Choi, M.-Y., Tatsuki, S., and Boo, K.-S. 1998. Regulation of sex pheromone biosynthesis in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Insect Physiol. 44: 653-658.
9. Crews, D. 1976. Hormonal control of male courtship behavior and female attractivity in the garter snake (Thamnophis radix). Horm. Behav. 7: 451-460.
10. Crews, D. and Moore, M. C. 1986. Evolution of mechanisms controlling mating behavior. Science 231: 121-125.
11. Duellman, W. E. and Trueb, L. 1994. Biology of Amphibians. Johns Hopkins University Press, Baltimore.
12. Foster, S. P. 2000. Periodicity of sex pheromone biosynthesis, release and degradation in the lightbrown apple moth, Epiphyas postvittana (Walker). Arch. Insect Biochem. Physiol. 43: 125-136.
13. Garstka, W. R., Camazine, B., and Crews, D. 1982. Interactions of behavior and physiology during the annual reproductive cycle of the red-sided garter snake (Thamnophis sirtalis parietalis). Herpetol. 38: 104-123.
14. Gerhardt, H. C. 1978. Temperature coupling in the vocal communication system of the gray tree frog, Hyla versicolor. Science 199: 992-994.
15. Gregory, P. T. 1976. Life-history parameters of the red-sided garter snake (Thamnophis sirtalis parietalis) in an extreme environment, the Interlake region of Manitoba. National Museum of Canada, Publications in Zoology 13: 1-44.
16. Hawley, A. W. and Aleksiuk, M. 1975. Thermal regulation of spring mating behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Can. J. Zool. 53: 768-776.
17. Hazel, J. R. and Williams, E. E. 1990. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog. Lipid Res. 29: 167-227.
18. Hoffmann, K. 1978. Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J. Reprod. Fertil. 54: 29-35.
19. Hudson, R. and Distel, H. 1990. Sensitivity of female rabbits to changes in photoperiod as measured by pheromone emission. J. Comp. Physiol. A 167: 225-230.
20. Iwata, T., Kawahara, G., Yamamoto, K., Zhou, C., Nakajo, S., Shioda, S., and Kikuyama, S. 2000a. Effect of prolactin and androgen on the expression of the female-attracting pheromone silefrin in the abdominal gland of the newt, Cynops ensicauda. Biol. Reprod. 63: 1867-1872.
21. Iwata, E., Wakabayashi, Y., Kakuma, Y., Kikusui, T., Takeuchi, Y., and Mori, Y. 2000b. Testosterone-dependent primer pheromone production in the sebaceous gland of male goat. Biol. Reprod. 62: 806-810.
22. Jacob, J., Balthazart, J., and Schoffeniels, E. 1979. Sex differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem. Syst. Ecol. 7: 149-153.
23. Jakobsson, A., Jorgensen, J. A., and Jacobsson, A. 2005. Differential regulation of fatty acid elongation enzymes in brown adipocytes implies a unique role for Elovl3 during increased fatty acid oxidation. Am. J. Physiol. Endocrinol. Metab. 289: E517-526.
24. Jakobsson, A., Westerberg, R., and Jacobsson, A. 2006. Fatty acid elongases in mammals: Their regulation and roles in metabolism. Prog. Lipid Res. 45: 237-249.
25. Kikuyama, S., Nakada, T., Toyoda, F., Iwata, T., Yamamoto, K., and Conlon, J. M. 2005. Amphibian pheromones and endocrine control of their secretion. Ann. N Y Acad. Sci. 1040: 123-130.
26. Kolattukudy, P. E. and Rogers, L. 1987. Biosynthesis of 3-hydroxy fatty acids, the pheromone components of female mallard ducks, by cell-free preparations from the uropygial gland. Arch. Biochem. Biophys. 252: 121-129.
27. Krohmer, R. W., Bieganski, G. J., Baleckaitis, D. D., Harada, N., and Balthazart, J. 2002. Distribution of aromatase immunoreactivity in the forebrain of redsided garter snakes at the beginning of the winter dormancy. J. Chem. Neuroanat. 23: 59-71.
28. Kubie, J. L., Cohen, J., and Halpern, M. 1978. Shedding enhances the sexual attractiveness of oestradiol treated garter snakes and their untreated penmates. Anim. Behav. 26: 562-570.
29. LeMaster, M. P. and Mason, R. T. 2001. Annual and seasonal variation in the female sexual attractiveness pheromone of the red-sided garter snake, Thamnophis sirtalis parietalis, pp. 369-376, in A. Marchlewska-Koj, J. Lepri, and D. Muller-Schwarze (eds.). Chemical Signals in Vertebrates 9. Kluwer Academic/Plenum, New York.
30. LeMaster, M. P. and Mason, R. T. 2002. Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J. Chem. Ecol. 28: 1269-1285.
31. LeMaster, M. P., Stefani, A., Shine, R., and Mason, R. T. 2008. Cross-dressing in chemical cues: Exploring 'she-maleness' in newly-emerged male garter snakes, pp. 223-230, in J. L. Hurst, R. J. Beynon, S. C. Roberts, and T. D. Wyatt (eds.). Chemical Signals in Vertebrates 11. Springer, New York.
32. Lutterschmidt, D. I. 2006. Chronobiology of garter snakes: environmental and hormonal mechanisms mediating hibernation and reproduction. Ph. D. dissertation, Oregon State University, Corvallis, OR.
33. Lutterschmidt, D. I., LeMaster, M. P., and Mason, R. T. 2006. Minimal overwintering temperatures of red-sided garter snakes (Thamnophis sirtalis parietalis): a possible cue for emergence? Can. J. Zool. 84: 771-777.
34. Maderson, P. F. A. 1986. The tetrapod epidermis: A system preadapted as a semiochemical source, pp. 13-25, in D. Duvall, D. Mueller-Schwarze, and R. M. Silverstein (eds.). Chemical Signals in Vertebrates 4. Plenum, New York.
35. Mason, R. T., Chinn, J. W., and Crews, D. 1987. Sex and seasonal differences in the skin lipids of garter snakes. Comp. Biochem. Physiol. B 87: 999-1003.
36. Mason, R. T., Fales, H. M., Jones, T. H., Pannell, L. K., Chinn, J. W., and Crews, D. 1989. Sex pheromones in snakes. Science 245: 290-293.
37. Mason, R. T., Jones, T. H., Fales, H. M., Pannell, L. K., and Crews, D. 1990. Characterization, synthesis, and behavioral responses to sex attractiveness pheromones of red-sided garter snakes (Thamnophis sirtalis parietalis). J. Chem. Ecol. 16: 2353-2369.
38. McCune, B., Grace, J. B., and Urban, D. L. 2002. Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, OR.
39. Mendonça, M. T. and Crews, D. 1996. Effects of ovariectomy and estrogen replacement on attractivity and receptivity in a dissociated pattern breeder, the red-sided garter snake (Thamnophis sirtalis parietalis). J. Comp. Physiol. A 178: 373-381.
40. Michael, R. P. 1975. Hormonal steroids and sexual communication in primates. J. Steroid Biochem. 6: 161-170.
41. Møller, A. P. and SzÉp, T. 2005. Rapid evolutionary change in a secondary sexual character linked to climatic change. J. Evol. Biol. 18: 481-495.
42. Moore, F. L. 1978. Effects of progesterone on sexual attractivity in female rough-skinned newts, Taricha granulosa. Copeia 1978: 530-532.
43. Mugford, R. A. and Nowell, N. W. 1971. Endocrine control over production and activity of the anti-aggression pheromone from female mice. J. Endocrinol. 49: 225-232.
44. Noble, G. K. 1937. The sense organs involved in the courtship of Storeria, Thamnophis and other snakes. Bull. Am. Mus. Nat. Hist. 73: 673-725.
45. Pandey, S. C. and Pandey, S. D. 1990. Role of photoperiod and temperature in production of the oestrus-inducing pheromone in male wild mice. Acta. Physiol. Hung. 76: 201-204.
46. Peltonen, L. M., Arieli, Y., Harjula, R., Pyörnilä, A., and Marder, J. 2000. Local cutaneous water barrier in cold- and heat-acclimated pigeons (Columba livia) in relation to cutaneous water evaporation. J. Morph. 246: 118-130.
47. Polak, M. and Starmer, W. T. 2005. Environmental origins of sexually selected variation and a critique of the fluctuating asymmetry-sexual selection hypothesis. Evolution 59: 577-585.
48. Pope, M. M., Gaston, L. K., and Baker, T. C. 1982. Composition, quantification, and periodicity of sex pheromone gland volatiles from individual Heliothis virescens females. J. Chem. Ecol. 8: 1043-1055.
49. Raina, A. K. and Klun, J. A. 1984. Brain factor control of sex pheromone production in the female corn earworm moth. Science 225: 531-533.
50. Raina, A., Jaffe, H., Kempe, T. G., Keim, P., Blacher, R. W., Fales, H. M., Riley, C. T., Klun, J. A., Ridgway, R. L., and Hayes, D. K. 1989. Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science 244: 796-798.
51. Rajchard, J. 2007. Intraspecific and interspecific chemosignals in birds: a review. Veterinarni Medicina 52: 385-391.
52. Ritchie, M. G., Saarikettu, M., Livingstone, S., and Hoikkala, A. 2001. Characterization of female preference functions for Drosophila montana courtship song and a test of the temperature coupling hypothesis. Evolution 55: 721-727.
53. Rust, C. C. and Meyer, R. K. 1969. Hair color, molt, and testis size in male, short-tailed weasels treated with melatonin. Science 165: 921-922.
54. Shimizu, I. and Barth, F. G. 1996. The effect of temperature on the temporal structure of the vibratory courtship signals of a spider (Cupiennius salei Keys). J. Comp. Physiol. A 179: 363-370.
55. Shine, R., Phillips, B., Waye, H., LeMaster, M. P., and Mason, R. T. 2003. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behav. Ecol. Sociobiol. 54: 162-166.
56. Sower, L. L., Shorey, H. H., and Gaston, L. K. 1971. Sex pheromones of noctuid moths. XXV. Effects of temperature and photoperiod on circadian rhythms of sex pheromone release by females of Trichoplusia ni. Ann. Entomol. Soc. Am. 27: 488-492.
57. Takahashi, N., Hasunuma, I., Iwata, T., Umezawa, K., Yamamoto, K., Marin, A., Perroteau, I., Vellano, C., and Kikuyama, S. 2001. Molecular cloning of newt prolactin (PRL) cDNA: effect of temperature on PRL mRNA expression. Gen. Comp. Endocrinol. 121: 188-195.
58. Thiessen, D. D., Friend, H. C., and Lindzey, G. 1968. Androgen control of territorial marking in the Mongolian gerbil. Science 160: 432-434.
59. Tiku, P. E., Gracey, A. Y., Macartney, A. I., Beynon, R. J., and Cossins, A. R. 1996. Cold-induced expression of delta9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271: 815.
60. Toyoda, F., Tanaka, S., Matsuda, K., and Kikuyama, S. 1994. Hormonal control of response to and secretion of sex attractants in Japanese newts. Physiol. Behav. 55: 569-576.
61. West, P. M. and Packer, C. 2002. Sexual selection, temperature, and the lion's mane. Science 297: 1339-1343.
62. Whittier, J. M. and Tokarz, R. 1992. Physiological regulation of sexual behavior in female reptiles, pp. 24-69, in C. Gans and D. Crews (eds.). Biology of the Reptilia. University of Chicago Press, Chicago.
63. Whittier, J. M., Mason, R. T., Crews, D., and Licht, P. 1987. Role of light and temperature in the regulation of reproduction in the red-sided garter snake, Thamnophis sirtalis parietalis. Can. J. Zool. 65: 2090-2096.
64. Willard, R., Packard, G. C., Packard, M. J., and Tucker, J. K. 2000. The role of the integument as a barrier to penetration of ice into overwintering hatchlings of the painted turtle (Chrysemys picta). J. Morph. 246: 150-159.
65. Yamamoto, K., Toyoda, F., Tanaka, S., Hayashi, H., and Kikuyama, S. 1996. Radioimmunoassay of a newt sex pheromone, Sodefrin, and the influence of hormones on its level in the abdominal gland. Gen. Comp. Endocrinol. 104: 356-363.