Pheromones and Reproduction in Garter Snakes

  • William R. Garstka
  • David Crews

Abstract

Darwin (1871) distinguished between sexual and natural selection, viewing them as separate, often apposing processes. Evolutionary biologists have shown how those behavioral traits associated with perpetuation of the individual’s genome, such as courtship displays, are under different selective pressures than are those associated with survival of the individual, such as thermoregulation. In the first instance, sexual selection may lead to conspicuous or extremely rapid evolution of a trait, whereas in the latter instance, natural selection will give rise to less dramatic and/or rapid changes (Arnold and Houck, 1982; Kirkpatrick, 1982; Lande, 1980, 1981).

Keywords

Cholesterol Permeability Estrogen Covariance Chloroform 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldridge, R. D., 1979, Female reproductive cycles of the snakes Arizona elegans and Crotalus viridis, Herpetologica, 35: 256.Google Scholar
  2. Aleksiuk, M ., 1975, Manitoba’s fantastic snake pits, Natl. Geogr., 147: 715.Google Scholar
  3. Aleksiuk, M., 1976, Reptilian hibernation: Evidence of adaptive strate¬gies in Thamnophis sirtalis parietalis, Copeia, 1976: 170.Google Scholar
  4. Aleksiuk, M., and Gregory, P. T., 1974, Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis, Copeia, 1976: 681.Google Scholar
  5. Ansari, A. Q., Dolphin, P. J., Lazier, C. B., Munday, K. A., and Akhtar, M., 1971, Chemical composition of an oestrogen-induced, calcium binding glycolipophosphoprotein in Xenopus laevis, Biochem..J., 122: 107.Google Scholar
  6. Arnold, S. J., 1983, Sexual selection: The interface of theory and empiricism, in: Mate Choice,11 P. Bateson, ed., Cambridge Univ. Press., Cambridge.Google Scholar
  7. Arnold, S. J., and Houck, L. D., 1982, Courtship pheromones: Evolution by natural and sexual selection, in: “Biochemical Aspects of Evolutionary Biology” M. H. Nitecki, ed., Univ. of Chicago Press, Chicago.Google Scholar
  8. Ball, R. L., 1979, “The Courtship and Mating Behavior of a Mexican Garter Snake, Thamnophis melanogaster” MS Diss., Univ. Oklahoma.Google Scholar
  9. Bermant, G., and Davidson, J. M., 1974, “Biological Bases of Sexual Behavior” Harper and Row, New York.Google Scholar
  10. Bishop, J. E ., 1959, A histological and histochemical study of the kidney tubule of the common garter snake, Thamnophis sirtalis, with special reference to the sexual segment in the male, J. Morphol., 104: 307.CrossRefGoogle Scholar
  11. Blanchard, F. N., and Blanchard, F. C., 1941a, Factors determining the time of birth in the garter snake Thamnophis sirtalis sirtalis ( Linnaeus ), Mich. Academic., 26: 161.Google Scholar
  12. Blanchard, F. N., and Blanchard, FC., 1941b, Mating of the garter snake Thamnophis sirtalis sirtalis ( Linnaeus ), Mich. Academic., 27: 215.Google Scholar
  13. Burghardt, G. M ., 1970, Chemical perception in reptiles, Adv. Chemorecept., 1: 241.Google Scholar
  14. Camazine, B., Garstka, W. R., Tokarz, R. 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.CrossRefGoogle Scholar
  15. Carpenter, C. C ., 1977, Communication and display of snakes, Am. Zool., 17: 217.Google Scholar
  16. Cieslak, E. S., 1945, Relation between the reproductive cycle and the pituitary gland in the snake Thamnophis radix, Physiol. Zool., 18: 299.Google Scholar
  17. Crews, D., 1975, Psychobiology of reptilian reproduction, Science, 189: 1059.Google Scholar
  18. Crews, D ., 1976, Hormonal control of male courtship behavior and female attractivity in the garter snake ( Thamnophis sirtalis sirtalis ), Horm. Behav., 7: 451.CrossRefGoogle Scholar
  19. Crews, D., 1983, Control of male sexual behavior in the Canadian red- sided garter snake, in: “Hormones and Behavior in Higher Verte¬brates” J. Balthazard, ed., Plenum Press, London.Google Scholar
  20. Crews, D ., 1984, Gamete production, sex steroid secretion, and mating behavior uncoupled, Horm. Behav., 18: 21.Google Scholar
  21. Crews, D. and Garstka, W. R., 1982, The ecological physiology of a garter snake, Sei. Am. 247: 158.Google Scholar
  22. Crews, D., Camazine, B., Diamond, M., Mason, R., Tokarz, R. R., and Garstka, W. R., 1984, Hormonal independence of courtship behavior in the male garter snake, Horm. Behav., 18:29.Google Scholar
  23. Garstka, W. R ., 1984, Hormonal independence of courtship behavior in the male garter snake, Horm. Behav., 18: 29.Google Scholar
  24. Garstka, W. R ., 1984, Hormonal independence of courtship behavior in the male garter snake, Horm. Behav., 18: 29.Google Scholar
  25. Cuellar, H. S., Roth, J. J., Fawcett, J. D., and Jones, R. E., 1972, Evidence for sperm sustenance by secretions of the renal sex segment of male lizards, Anolis carolinensis, Herpetologica, 28:53.Google Scholar
  26. Darwin, C., 1871, “The Descent of Man and Selection in Relation to Sex” John Murray, London.Google Scholar
  27. Devine, M. C ., 1975, Copulatory plugs in snakes: Enforced chastity, Science, 187: 844.ADSCrossRefGoogle Scholar
  28. Devine, M. C., 1977a, Copulatory plugs, restricted opportunities, and reproductive competition among male garter snakes, Nature, 267: 345.Google Scholar
  29. Devine, M. C., 1977b, “Chemistry and Source of Sex-attractant Pheromones and Their Role in Mate Discrimination by Garter Snakes” Ph.D. Diss.. Univ. Michigan.Google Scholar
  30. Emlen, S. T., and Oring, L. W., 1977, Ecology, sexual selection, and the evolution of mating systems, Science, 197: 215.ADSCrossRefGoogle Scholar
  31. Farner, D. S., and Follett, B. K., 1979, Reproductive periodicity in birds, In: “Hormones and Evolution” E. J. W. Barrington, ed., Academic Press, New York.Google Scholar
  32. Fitch, H. S., 1965, An ecological study of the garter snake, Thamnophis sirtalis, Univ. Kans. Publ. Mus. Nat. Hist., 15: 493.Google Scholar
  33. Ford, N. B ., 1978, Evidence for species specificity of pheromone trails in two sympatric garter snakes, Thamnophis, Herpetol. Rev., 9: 10.Google Scholar
  34. Ford, N. B ., 1981, Seasonality of pheromone trailing behavior in two species of garter snake, Thamnophis ( Colubridae ), Southwest, Nat., 26: 385.CrossRefGoogle Scholar
  35. Ford, N. B., 1982, Species specificity of sex pheromone trails of sympatric and allopatric garter snakes ( Thamnophis ), Copeia, 1982: 10.Google Scholar
  36. Ford, N. B., and Ball, R., 1977, Clutch size and size of young in the Mexican garter snake, Thamnophis melanogaster (Reptilia, Serpentes, Colubridae ), Herpetol. Rev., 8: 118.Google Scholar
  37. Fox, H., 1979, The urinogenital system of reptiles, in: “Biology of the Reptilia” Vol. 7, C. Gans, ed., Academic Press, New York.Google Scholar
  38. Fox, W., 1952, Seasonal variation in the male reproductive system of Pacific coast garter snakes, J. Morphol., 90: 481.CrossRefGoogle Scholar
  39. Fox, W., 1954, Genetic and environmental variation in the timing of the reproductive cycle of male garter snakes, J. Morphol., 95: 415.CrossRefGoogle Scholar
  40. Fox, W ., 1956, Seminal receptacles of snakes, Anat. Rec., 124: 519.CrossRefGoogle Scholar
  41. Friedman, D. W., and Crews, D., 1985a, Role of the anterior hypothalamale Canadian red-sided garter snake (Thamnophis sirtalis parietalis): Intracranial implantation experiments, Horm. Behav., (in press)Google Scholar
  42. Gapp, D. A., Ho., S-m., and Callard, I. P., 1979, Plasma levels of vitellogenin in Chrysemys picta during the annual gonadal cycle: Measurement by specific radioimmunoassay, Endocrinology, 104: 784.Google Scholar
  43. Gardner, J. B., 1955, A ball of snakes, Copeia, 1955: 310.Google Scholar
  44. Gardner, J. B., 1957, A garter snake ball, Copeia, 1957: 48.Google Scholar
  45. Garstka, W. R., 1982, “Chemical Communication and the Control of Garter Snake Reproductive Cycles” Ph.D. Diss., Harvard Univ.Google Scholar
  46. Garstka, W. R., and Crews, D., 1981, Female sex pheromone in the skin and circulation of a garter snake, Science, 214: 681.ADSCrossRefGoogle Scholar
  47. Garstka, W. R., and Crews, D., 1982, Female control of male reproductive function in a Mexican snake, Science, 217: 1159.ADSCrossRefGoogle Scholar
  48. Garstka, W. R., and Crews, D., 1985, Mate preference in garter snakes. Herpetologica, 41: 9.Google Scholar
  49. Garstka, W. R., Camazine, B., and Crews, D., 1982, Interaction of behavior and physiology during the annual reproductive cycle of the red-sided garter snake ( Thamnophis sirtalis parietalis ), Herpetologica, 38: 104.Google Scholar
  50. Garstka, W. R., and Crews, D., 1985, Mate preference in garter snakes. Herpetologica, 41:9.Google Scholar
  51. Gehlbach, F. R., Watkins, J. F., and Kroll, J. C., 1971, Pheromone trail-following studies of typhlopid, leptotyphlopid, and colubrid snakes, Behaviour, 40: 282.CrossRefGoogle Scholar
  52. Gillingham, J. C., and Clark, D. L., 1981, An analysis of prey searching behavior in the western diamondback rattlesnake, Crotalus atrox, Behav. Neural Biol., 32: 235.CrossRefGoogle Scholar
  53. Gillingham, J. C., and Dickinson, J. A., 1980, Postural orientation during courtship in the eastern garter snake, Thamnophis s. sirtalis, Behav. Neural Biol., 28: 211.CrossRefGoogle Scholar
  54. Guillette, L. J., 1982, The evolution of viviparity and placentation in the high elevation Mexican lizard Sceloporus aeneus, Herpetologica, 38: 94.Google Scholar
  55. Gregory, P. T., 1974, Patterns of spring emergence of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake region of Manitoba, Can. J. Zool., 52:1063.Google Scholar
  56. Gregory, P. T., 1977, Life history parameters of the red-sided garter snake ( Thamnophis sirtalis parietalis) in an extreme environment, the Interlake region of Manitoba, Natl. Mus. Nat. Sei. Ottawa Publ. Zool. No. 13.Google Scholar
  57. Gupta, SC., Thapliyal, JP., and Garg, RK., 1975, The effects of Thyroid hormones on the chemical constituents of different tissues of the chequered water snake Natrix piscator, Gen. Comp. Endocrinol., 27: 223.CrossRefGoogle Scholar
  58. Halliday, T. R., 1978, Sexual selection and mate choice, in: “Behavioural Ecology; An Evolutionary Approach” J. R. Krebs, and N. B. Davies, eds., Blackwell Scientific Pubis., London.Google Scholar
  59. Halliday, T. R., 1983, The study of mate choice, in: “Mate Choice” P. Bateson, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  60. Halpert, AP., Garstka, W. R., and Crews, D., 1982, Sperm storage and transport and its relation to the annual sexual cycle of the female red-sided garter snake, Thamnophis sirtalis parietalis, J. Morphol., 174: 149.CrossRefGoogle Scholar
  61. Hawley, A.W.L., and Aleksiuk, M., 1975, Thermal regulation of spring mating behavior in the red-sided garter snake ( Thamnophis sirtalis parietalis ), Can. J. Zool., 53: 768.CrossRefGoogle Scholar
  62. Hawley, A. W. L., and Aleksiuk, M., 1976, The influence of photoperiod and temperature on seasonal testicular recrudescence in the red- sided garter snake ( Thamnophis sirtalis parietalis ), Comp. Biochem. Physiol., A53: 215CrossRefGoogle Scholar
  63. Heisermann, G. J., 1982, “An Estrogen Receptor in the Liver of the Turtle, Chrysemys picta” M.A. Diss., Boston Univ.Google Scholar
  64. Heisermann, GJ., Ho, SM., and Callard, IP., 1980, Identification of an estrogen receptor in the liver cytosol of a turtle, Chrysemys Picta Am. Zool., 20: 792Google Scholar
  65. Hiller, U ., 1971, Form und Funktion der Hautsinnesorgane bei Gekkoniden, 1. Licht und Raterelecktronenmikroskopie Untersuchungen, Form. Funct., 4: 240.Google Scholar
  66. Hoffman, LH ., 1970, Placentation in the garter snake, Thamnophis sirtalis, J. Morphol., 131: 57.CrossRefGoogle Scholar
  67. Jackson, M. K., and Sharawy, M., 1978, Lipids and cholesterol clefts in the lacunar cells of snake skin, Anat. Ree., 190: 41.CrossRefGoogle Scholar
  68. Joy, J., and Crews, D., 1985, Social facilitation of courtship behavior in the red-sided garter snake, Thamnophis sirtalis parietalis, J. Comp. Psychol., (in press).Google Scholar
  69. Karlson, P., and Schneider, D., 1973, Sexual hormone der Schmetterlinge als Modelle chemischer Kommunikation, Naturwissenschaften, 60:113.ADSCrossRefGoogle Scholar
  70. Kirkpatrick, M. , 1982, Sexual selection and the evolution of female choice, Evolution, 36:1.CrossRefGoogle Scholar
  71. Kittredge, J. S., and Takahashi, F. T., 1972, The evolution of sex pheromone communication in the arthropoda, J. Theor. Biol. 35:467.CrossRefGoogle Scholar
  72. Kubie, J. L., 1977, “The Role of the Vomeronasal Organ in Garter Snake Prey Trailing and Courtship,”: Ph.D. Diss., S.U.N.Y.Google Scholar
  73. Kubie, J. L., Vagvolgyi, A., and Halpern, M., 1978a, Roles of the vomeronasal and olfactory systems in courtship behavior of male garter snakes, J. Comp. Physiol. Psychol., 92:627.CrossRefGoogle Scholar
  74. Kubie, J. L., Cohen, J., and Halpern, M., 1978b, Shedding enhances the attractiveness of oestradiol treated garter snakes and their untreated penmates, Anim. Behav., 26:562.CrossRefGoogle Scholar
  75. Lande, R.,1980, Sexual dimorphism, sexual selection, and adaptation in polygenic characters, Evolution, 34:292.CrossRefGoogle Scholar
  76. Lande, R., 1981, Models of speciation by sexual selection of polygenic traits, Proc. Natl. Acad. Sci., 78:3721.MathSciNetADSCrossRefGoogle Scholar
  77. Landmann, L., 1975, The sense organs in the skin of the head of squamata (Reptilia), Israel J. Zool., 24:99.Google Scholar
  78. Landmann, L., 1979, Keratin formation and barrier mechanisms in the epidermis of Natrix natrix (Reptilia: Serpentes): An ultrastructural study, J. Morphol., 162:93. CrossRefGoogle Scholar
  79. Landmann, L., 1980, Zonulae occulodentes in the epidermis of the snake Natrix natrix L., Experientia, 36:110.CrossRefGoogle Scholar
  80. Landmann, L., Stolinski, C., and Martin, B., 1981, The permeability barrier in the epidermis of the grass snake during the resting stage of the sloughing cycle, Cell Tissue Res., 215:369.Google Scholar
  81. List, J. C., 1950, Observations on the courtship behavior of Thamnophis sirtalis sirtalis, Herpetologica, 6:71.Google Scholar
  82. Maderson, P. F. A., 1965, Histological changes in the epidermis of snakes during the sloughing cycle, J. Zool., 146:98.Google Scholar
  83. Maderson, P. F. A., 1984, Some developmental problems of the reptilian integument, in: “Biology of the Reptilia,” (in press).Google Scholar
  84. Maderson, P. F. A., Chiu, K. W., and Phillips, J. G., 1970a, Changes in the epidermal histology during the sloughing cycle in the rat snake Ptyas korros Schlegel, with correlated observations on the thyroid gland, Biol. Bull., 139:304.Google Scholar
  85. Maderson, P. F. A., Chiu, K. W., and Phillips, J. G., 1970b, Endocrine-epidermal relationships in squamate reptiles, Mem. Soc. Endocrinol., 18:259.Google Scholar
  86. Meredith, M., and Burghardt, G. M., 1978, Electrophysiological studies of the tongue and accessory olfactory bulb in garter snakes, Physiol. Behav., 21:1001.CrossRefGoogle Scholar
  87. Muller-Schwarze, D., and Mozell, M. M., 1977, “Chemical Signals in Vertebrates,” Plenum Press, New York.Google Scholar
  88. Mulner, O., and Ozon, R., 1981, The roles of the follicular envelopes in the initiation of Xenopus oocyte maturation, Gen. Comp. Endocrinol., 44:335.CrossRefGoogle Scholar
  89. Munro, D. F., 1948, Mating behavior and seasonal cloacal discharge of a female Thamnophis sirtalis parietalis, Herpetologica, 4:185.Google Scholar
  90. Nakamura, K., 1935, On a new integumental poison gland found in the nuchal region of a snake, Natrix tigrina, Mem. Coll. Sci. Univ., Kyoto Ser. B., 10:229.Google Scholar
  91. Noble, G. K., 1937, The sense organs involved in the courtship of Storeria, Thamnophis, and other snakes, Bull. Am. Mus. Nat. Hist., 73:673. Google Scholar
  92. Orians, G. H., 1969, On the evolution of mating systems in birds and mammals, Am. Nat., 103:589.CrossRefGoogle Scholar
  93. Pisani, G. R., 1976, Comments on the courtship and mating mechanics of Thamnophis (Reptilia, Serpentes, Colubridae), J. Herpetol., 10:139.Google Scholar
  94. Prasad, M. R. N., and Reddy, PRK., 1972, Physiology of the sexual segment of the kidney in reptiles, Gen. Comp. Endocrinol., Suppl. 3: 649.CrossRefGoogle Scholar
  95. Rahn, H., 1940, Sperm viability in the uterus of the garter snake, Thamnophis, Copeia, 1940: 109.Google Scholar
  96. Rauch, JC ., 1978, Integumentary bloodvascular system in garter snakes (Thamnophis sirtalis parietalis and. radix ), Can. J. Zool., 56: 469CrossRefGoogle Scholar
  97. Regaud, C., and Policard, A., 1903, Variations sexuelles de structure dans le segment preterminal du tube urinifere de quelques ophidiens, C. R. Soc. de Biol. ( Paris ), 55: 216.Google Scholar
  98. Roberts, J. B., and Lillywhite, H. B., 1980, Lipid barrier to water exchange in reptile epidermis, Science, 207: 1077.ADSCrossRefGoogle Scholar
  99. Ross, P., and Crews, D., 1977, Influence of the seminal plug on mating behavior in the garter snake, Nature, 267: 344.ADSCrossRefGoogle Scholar
  100. Ross, P., and Crews, D., 1978, Stimuli influencing mating behavior in the garter snake, Thamnophis radix, Behav. Ecol. Sociobiol., 4: 133.CrossRefGoogle Scholar
  101. Rossman, D. A., and Eberle, W. G., 1977, Partition of the genus Natrix, with preliminary observations on evolutionary trends in natricine snakes, Herpetologica, 33: 34.Google Scholar
  102. Ruthven, A. G., 1908, Variation and genetic relationships of the garter snakes, Bull. U.S. Natl. Mus., 61: 1.Google Scholar
  103. Smith, G. C., 1976, Ecological energetics of three species of ecto- thermic vertebrates, Ecology, 57: 252.CrossRefGoogle Scholar
  104. Smith, HM ., 1942, The synonymy of the garter snakes ( Thamnophis), with notes on Mexican and Central American species, Zoologica, 27: 97Google Scholar
  105. Smith, MA ., 1938, The nucho-dorsal glands of snakes, Proc. Zool. Soc., Lond., 108: 575Google Scholar
  106. Stewart, G. R., 1972, An unusual record of sperm storage in a garter snake (genus Thamnophis), Herpetologica, 28: 346.Google Scholar
  107. Stokes, GP., and Dunson, WA., 1982, Permeability and channel structure of reptilian skin, Am. J. Physiol., 242: 681.Google Scholar
  108. Wade, G. N., and Gray, J. M., 1978, Cytoplasmic 173-(3H) estradiol binding in rat adipose tissues, Endocrinology, 103: 1695.CrossRefGoogle Scholar
  109. Wallace, R. A., 1979, Oocyte growth in nonmammalian vertebrates, in: The Vertebrate Ovary,11 R. E. Jones, ed., Plenum Press, New York.Google Scholar
  110. Wallace, RA., and Bergink, EW., 1974, Amphibian vitellogenin: Properties, hormonal regulation of hepatic synthesis and ovarian uptake, and conversion to yolk platelets, Am. Zool., 14: 1159Google Scholar
  111. White, F. N., 1957, A functional interpretation of the integumentary vessels of snakes, Herpetologica, 13: 127.Google Scholar
  112. Whittier, J., and Crews, D., 1985, Variation in reproductive patterns of female red-sided garter snakes, Thamnophis sirtalis parietalis, Anim. Behav., (in press).Google Scholar
  113. Whittier, J. M., Mason, R. T., and Crews, D., 1985, Sexual selection and the effects of mating on sexual behavior in the red-sided garter snake, Thamnophis sirtalis parietalis, Behav. Ecol. Sociobiol., (in press).Google Scholar
  114. Zahavi, A., 1975, Mate selection - a selection for a handicap, J. Theor. Biol., 53:205.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • William R. Garstka
    • 1
  • David Crews
    • 2
  1. 1.Dept. Biol. Sci.University of AlabamaHuntsvilleUSA
  2. 2.Inst. Reprod. BiolUniversity of TexasAustinUSA

Personalised recommendations