Fossil and Comparative Evidence for Possible Chemical Signaling in the Mammal-Like Reptiles

  • David Duvall
  • Michael B. King
  • Brent M. Graves


The mammal-like reptiles, or the Synapsida, hold an important position in the study of tetrapod vertebrate evolution for several reasons. First, the pelycosaurs and their therapsid derivatives, the two groups that comprise the synapsids, probably evolved from the cotylosaurs (the “stem reptiles”) (Carroll, 1969), and gave rise much later to the mammals (Fig. 1). Indeed, the mammal-like reptiles were the dominant terrestrial tetrapods throughout the Permian and the Triassic, the period from roughly 300 to 190 million years ago (Romer, 1966). Given this position in phylogeny, these extinct members of the Class Reptilia have always held the interest of those interested in the origins and derivation of mammals (e.g., see Simpson, 1959; Crompton and Jenkins, 1979).


Chemical Signal Vomeronasal Organ Garter Snake Skin Gland Secondary Palate 
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  1. Allison, A.C., 1953, The morphology of the olfactory system in the vertebrates, Biol. Rev., 28: 195–244.CrossRefGoogle Scholar
  2. Atz, J.W., 1970, The application of the idea of homology to behavior, in: “Development and Evolution of Behavior,” L.R. AronsonGoogle Scholar
  3. E. Tobach, D.S. Lehrman, and J.S. Rosenblatt, eds., W.H. Freeman, San Francisco.Google Scholar
  4. Auffenberg, W., 1978, Social and feeding behavior of Varanus komodoensis, in: “Behavior and Neurology of Lizards,” N. Greenberg, and P.D. MacLean, eds., NIMH, Poolesville, Maryland.Google Scholar
  5. Bakker, R.T., 1980, Dinosaur heresy-dinosaur renaissance: Why we need endothermic archosaurs for a comprehensive theory of bio-energetic evolution, in: “A Cold Look at the Warm-blooded Dinosaurs,” D.K. Thomas and E.C. Olson, eds., Westview Press, Boulder.Google Scholar
  6. Bennett, A.F., and Ruben, J., 1982, Ambient temperature and evol-ution of basal metabolic rate during the reptilian-mammalian transition, in: “The Paleobiology of the Mammal-like Reptiles,” J.J. Roth, E.C. Roth, N.H. Hotton, and P.D. MacLean, eds., The Smithsonian Institution Press, Washington, D.C., In Press.Google Scholar
  7. Berry, K.H., 1974, The ecology and social behavior of the chuckwalla, Sauromalus obesus obesus Baird, Univ. California Publ. Zool., 101: 1–60.Google Scholar
  8. Bertmar, G., 1981, Evolution of vomeronasal organs in vertebrates, Evolution, 35: 359–366.CrossRefGoogle Scholar
  9. Blass, E.M., and Teicher, M.H., 1980, Suckling, Science, 210: 15–22.ADSCrossRefGoogle Scholar
  10. Block, M.L., Volpe, L.C.,and Hayes, M.J., 1981, Saliva as a chemical cue in the development of social behavior, Science, 211: 1062–1064.ADSCrossRefGoogle Scholar
  11. Boyden, A., 1947, Homology and analogy, a critical review of the meanings and implications of these concepts in biology, Amer. Midl. Nat., 37: 648–669.CrossRefGoogle Scholar
  12. Brink, A.S., 1957, Speculations on some advanced mammalian characteristics in the higher mammal-like reptiles, Palaeontol. Afr. 4: 77–96.Google Scholar
  13. Broman, I., 1920, Das Organon vomero-nasale Jacobsoni,ein Wassergeruchsorgan:, Anat. Hefte., 58: 137–191.CrossRefGoogle Scholar
  14. Broom, R., 1937, On the palate, occiput and hind foot of Bauria cynops Broom, Amer. Mus. Nov., No. 946: 1–6.Google Scholar
  15. Burghardt, G.M., 1980, Behavioral and stimulus correlates of vomero- nasal functioning in reptiles: Feeding, grouping, sex, and tongue use, in: “Chemical Signals,” D. Müller-Schwarze, and R.M. Silverstein,eds., Plenum, New York.Google Scholar
  16. Carroll, R.L., 1969, Origin of reptiles, in: “Biology of the Reptilia, Vol. 1,” C. Gans, A.d’A. Bellairs, and T.S. Parsons, eds., Academic Press, New York.Google Scholar
  17. Chudinov, P.K., 1968, Structure of the integuments of theriomorphs. Doklady Acad. Nauk SSSR, 179: 207–210. (Translation by Amer. Geol. Inst.)Google Scholar
  18. Colbert, E.H., 1958, Morphology and behavior, in: “Behavior and Evolution,” A. Roe, and G.G. Simpson, eds., Yale University Press, New Haven, Connecticut.Google Scholar
  19. Cowles, R.B., and Phelan, R.L., 1958, Olfaction in rattlesnakes, Copeia, 1958: 77–83.CrossRefGoogle Scholar
  20. Cluver, M.A., 1971, The cranial morphology of the dicynodont genus Lystrosaurus, Ann. S. Afr. Mus., 56: 155–274.Google Scholar
  21. Crompton, A.W., and Jenkins, F.A., 1979, Origin of mammals, in: “Mesozoic Mammals,” J.A. Lillegraven, Z. Kielanaworowska, and W.A. Clemans, eds., University of California Press, Berkeley.Google Scholar
  22. Darwin, C., 1859, “The Origin of Species by Means of Natural Selection,or ”The Preservation of Races in the Struggle for Life,“ Reprinted by Doubleday and Co., Inc., Garden City, New York, 1960.Google Scholar
  23. Duvall, D., 1979, Western fence lizard (Sceloporus ccidentalis) chemical signals. I. Conspecific discriminations and release of a species-typical visual display, J. Exp. Zool., 210: 321–326.CrossRefGoogle Scholar
  24. Duvall, D., 1981, Western fence lizard (Sceloporusoccidentalis) chemical signals. II. A replication with naturally breeding adults and a test of the Cowles and Phelan hypothesis of rattlesnake olfaction, J. Exp. Zool., 218: 351–361.CrossRefGoogle Scholar
  25. Duvall, D., 1982a, A new question of pheromones: Aspects chemical signaling and reception in the mammal-like in: “The Paleobiology of the Mammal-like Reptiles,” E.C. Roth, N.H. Hotton, and P.D. MacLean, eds., The ian Institution Press, Washington, D.C., In Press. of possible reptiles, J.J. Roth, Smithson-Duvall, D., 1982b, Western fence lizard (Sceloporus occidentalis) chemical signals. III. An experimental ethogram of conspecific body licking, J. Exp. Zool., In press.Google Scholar
  26. Duvall, D., Guillette, L.J., Jr., and Jones, R.E., 1982, Environmental control of reptilian reproductive cycles, in: “Biology of the Reptilia, Vol. 12,” C. Gans, and F.H. Pough,eds., Academic Press, London, In Press.Google Scholar
  27. Duvall, D., Herskowitz, R.L., and Trupiano-Duvall, J., 1980, Responses of five-lined skinks (Eumeces fasciatus) and ground skinks (Scincella lateralis) to conspecific and interspecific chemical cues, J. Herpetol., 14: 121–127.CrossRefGoogle Scholar
  28. Duvall, D., Trupiano, J., and Smith, H.M., 1979, An observation of maternal behavior in the Mexican desert spiny lizard, Sceloporus rufidorsum, Trans., Kansas Acad, Sci., 82: 60–62.CrossRefGoogle Scholar
  29. Eisenberg, J.F., and Kleiman, D.G., 1972, Olfactory communication in mammals, in: “Annual Review of Ecology and Systematics, Vol. 3,” R.F. Johnston, P.W. Frank, and C.D. Michener, eds., Annual Reviews, Inc., Palo Alto, California.Google Scholar
  30. Estes, R.D., 1972, The role of the vomeronasal organ in mammalian reproduction, Mammalia, 36: 315–341.CrossRefGoogle Scholar
  31. Evans, L.T., 1959, A motion picture study of maternal behavior of the lizard, Eumeces obsoletus Baird and Girard, Copeia, 1959: 103–110.CrossRefGoogle Scholar
  32. Fitch, H.S., 1954, Life history and ecology of the five-lined skink, Eumeces fasciatus, Univ. Kansas Publ. Mus. Nat. Hist., 8: 11–56.Google Scholar
  33. Galton, P.M., 1970, Pachycephalosaurids-dinosaurian battering rams, Discovery, 6: 23–32.Google Scholar
  34. Garstka, W.R., and Crews, D., 1981, Female sex pheromone in the skin and circulation of a garter snake, Science, 214: 681–683.ADSCrossRefGoogle Scholar
  35. Graves, B., Galvin, R., and Duvall, D., Under Review, Chemical signals as the immediate preadaption for neonate utilization of skin gland nutritive secretions, Evolution.Google Scholar
  36. Greene, H.W., and Burghardt, G.M., 1978, Behavior and phylogeny: Constriction in ancient and modern snakes, Science, 200: 74–77.ADSCrossRefGoogle Scholar
  37. Grine, F.E., Mitchell, D., Gow, C.E., Kitching, J.W., and Turner, B.R., 1979, Evidence for salt glands in the Triassic reptile Diademodon (Therapsida: Cynodontia), Palaeont. Afr., 22: 35–39.Google Scholar
  38. Guillette, L.J.,Jr., 1982, The evolution of viviparity and placentation in reptiles: An hypothesis for the evolution of viviparity in mammal-like reptiles, in: “The Paleobiology of the Mammal-like Reptiles,” J.J. Roth, E.C. Roth, N.H. Hotton, and P.D. MacLean, eds., The Smithsonian Institution Press, Washington, D.C., In Press.Google Scholar
  39. Hopson, J.A., 1973, Endothermy, small size, and the origin of mammalian reproduction, Amer. Nat., 107: 446–452.CrossRefGoogle Scholar
  40. Halpern, M., 1976, The efferent connections of the olfactory bulb and accessory olfactory bulb in the snakes, Thamnophis sir-talis and Thamnophis radix, J. Morphol., 150: 553–578.Google Scholar
  41. Halpern, M., 1980, The telencephalon of snakes, in: “Comparative Neurology of the Telencephalon,” S.O.E. Ebbesson, ed., Plenum, New York.Google Scholar
  42. Halpern, M., and Frumin, N., 1979, Roles of the vomeronasal and olfactory systems in prey attack and feeding in adult garter snakes, Physiol. Behay., 22: 1183–1189.CrossRefGoogle Scholar
  43. Heller, S.B., and Halpern, M., Under Review, Laboratory observations of aggregative behavior of garter snakes, Thamnophis sirtalis: The roles of visual, olfactory and vomeronasal senses, J. Comp. Physiol. Psychol.Google Scholar
  44. Hofer, M.A., Shair, H., and Singh, P.J., 1976, Evidence that maternal ventral skin substances promote suckling in infant rats, Physiol. Behay., 17: 131–136.CrossRefGoogle Scholar
  45. Hopson, J.A.,1975, The evolution of cranial display structures in hadrosaurian dinosaurs, Paleobiology, 1: 21–43.Google Scholar
  46. Hotton, N.H., 1982, Dicynodonts and other primary consumers, in: “The Paleobiology of the Mammal-like Reptiles,” J.J. Roth, E.C. Roth, N.H. Hotton, and P.D. MacLean, eds., The Smithsonian Institution Press, Washington, D.C., In Press.Google Scholar
  47. Jacobson, L., 1811, Description anatomique d’un organ observé dans les mammifbres, Ann. du Mus. d’Hist. Nat. Paris., 18: 412–424.Google Scholar
  48. Jerison, H.J., 1973, “Evolution of the Brain and Intelligence,” Academic Press, New York.Google Scholar
  49. Johns, M.A., 1980, The role of the vomeronasal system in mammalian reproductive physiology, in: “Chemical Signals,” D. Müller-Schwarze, and R.M. Silverstein, eds., Plenum, New York.Google Scholar
  50. Johns, M.A., Feder, H.H., Komisaruk, B.R., and Mayer, A.D., 1978, Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect, Nature, 272: 446–448.ADSCrossRefGoogle Scholar
  51. Kemp, T.S., 1979, The primitive cynodont Procynosuchus: Functional anatomy of the skull and relationships, Phil. Trans, Royal Soc London, B. Biol. Sci., 285: 73–122.ADSCrossRefGoogle Scholar
  52. King, G.M., 1981, The functional anatomy of a Permian dicynodont, Phil. Trans. Royal Soc. London, B. Biol. Sci., 291: 243–322.ADSCrossRefGoogle Scholar
  53. King, M.B., McCarron, D., Duvall, D., Baxter, G., and Gern, W., Under Review, Avoidance of conspecific but not interspecific chemical signals by prairie rattlesnakes, Crotalus viridis viridis, J. Herpetol.Google Scholar
  54. Kubie, J.L. and Halpern, M., 1979, Chemical senses involved in garter snake prey trailing, J. Comp. Physiol. Psychol., 93: 648–667.CrossRefGoogle Scholar
  55. Kubie, J.L., Vagvolgyi, A., and Halpern, M., 1978, Roles of the vomeronasal and olfactory systems in courtship behavior of male garter snakes, J. Comp. Physiol. Psychol., 92: 627–641.CrossRefGoogle Scholar
  56. Leon, M, 1979, Mother-young reunions, in: “Progress in Psychobiology and Physiological Psychology, Vol 8,” J.M. Sprague, and A.N. Silverstein, eds., Academic Press, New York.Google Scholar
  57. Lillegraven, J.A., 1979, Reproduction in Mesozoic mammals, in: “Mesozoic Mammals,” J.A. Lillegraven, Z. Kielan-Jaworowska, and W.A. Clemens, eds., The University of California Press, Berkeley.Google Scholar
  58. Long, C.A., 1969, The origin and evolution of mammary glands, Bioscience, 19: 519–523.CrossRefGoogle Scholar
  59. MacLean, P.D., 1978, Why brain research on lizards?, in: “Behavior and Neurology of Lizards,” N. Greenberg, and P.D. MacLean, eds., NIMH, Poolesville, Maryland.Google Scholar
  60. Madison, D.M., 1977, Chemical communication in amphibians and reptiles, in: “Chemical Signals,” D. Müller-Schwarze, and M.M. Mozell, eds., Plenum, New York.Google Scholar
  61. Meredith, M., 1980, The vomeronasal organ and accessory olfactory system in the hamster, in: “Chemical Signals,” D. Müller-Schwarze and R.M. Silverstein, eds., Plenum, New York.Google Scholar
  62. Molnar, R.E., 1977, Analogies in the evolution of combat and display structures in ornithopods and ungulates, Evol. Theory, 3: 165–190.Google Scholar
  63. Negus, V., 1958, “The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses,” Livingstone Ltd., Edinburgh and London.Google Scholar
  64. Noble, G.K., and Mason, E.R., 1933, Experiments on the brooding habits of the lizards Eumeces and Ophisaurus, Amer. Mus. Novitates, 619: 1–29.Google Scholar
  65. Olson, E.C. 1959, The evolution of mammalian characteristics, Evolution, 13: 344–353.CrossRefGoogle Scholar
  66. Parsons, T.S., 1959a, Nasal anatomy and the phylogeny of reptiles, Evolution, 13: 175–187.CrossRefGoogle Scholar
  67. Parsons, T.S., 1959b, Studies on the comparative embryology of the reptilian nose, Bull. Mus. Comp. Zool., Harvard Univ., 120: 101–277.Google Scholar
  68. Parsons, T.S., 1967, Evolution of the nasal structure in the lower tetrapods, Amer. Zool., 7: 397–413.Google Scholar
  69. Parsons, T.S., 1970, The nose and Jacobson’s organ, in: “Biology of the Reptilia, Vol. 2, Morphology B,” C. Gans and T.S. Parsons, eds., Academic Press, London.Google Scholar
  70. Parsons, T.S., 1971, Anatomy of nasal structures from a comparative viewpoint, in: “Handbook of Sensory Physiology, Vol. IV, Chemical Senses, Part 2, Olfaction,” L.M. Beidler, eds., Springer-Verlag, New York.Google Scholar
  71. Poduschka, W., 1977, Insectivore communication, in: “How Animals Communi- cate,” T.A. Seboek, ed., Indiana University Press, Bloomington.Google Scholar
  72. Poduschka, W., and Firbas, W., 1968, Das Selbstbespeicheln des Igels, Erinaceus europaeus Linnè, 1758, steht in Verbindung zur Funktion des Jacobsonschen Organes, Z. Säugetierk., 33: 160–172.Google Scholar
  73. Pond, C.M., 1977, The significance of lactation in the evolution of mammals, Evolution, 31: 177–199.CrossRefGoogle Scholar
  74. Porter, R.H., and Czaplicki, J.A., 1974, Response of water snakesGoogle Scholar
  75. Natrix r. rhombifera) and garter snakes (Thamnophis sirtalis) to chemical cues, Anim. Learn. Behay. 2:129–132.Google Scholar
  76. Powers, J.B., and Winans, S.S., 1975, Vomeronasal organ: Critical role in mediating sexual behavior in the male hamster, Science, l87: 961–963.ADSCrossRefGoogle Scholar
  77. Romer, A.S., 1959, “The Vertebrate Story,” The University of Chicago Press, Chicago.Google Scholar
  78. Romer, A.S., 1966, “Vertebrate Paleontology,” 3rd Ed., The University of Chicago Press, Chicago.Google Scholar
  79. Romer,A.S., and Parsons, T.S., 1977, “The Vertebrate Body,” 5th Ed., Saunders College Publishing, Philadelphia.Google Scholar
  80. Ross, P., Jr., and Crews, D., 1977, Influence of the seminal plug on mating behaviour in the garter snake, Nature, 267: 344–345.ADSCrossRefGoogle Scholar
  81. Roth, J.J., Roth, E.C., Hotton, N.H., and MacLean, P.D., eds., 1982, “The Paleobiology of the Mammal-like Reptiles,” The Smithsonian Institution Press, Washington, D.C., In press.Google Scholar
  82. Shorey, H.H., 1976, “Animal Communication by Pheromones,” Academic Press, New York.Google Scholar
  83. Simon, C.A., In press, Lizard Chemoreception: A review, Amer. Zool.Google Scholar
  84. Simpson, G.G., 1959, Mesozoic mammals and the polyphyletic origin of mammals, Evolution, 13: 405–414.CrossRefGoogle Scholar
  85. Simpson, G.G., 1961, “Principles of Animal Taxonomy,” Columbia University Press, New York.Google Scholar
  86. Singh, P.J., and Hofer, M.A., 1978, Oxytocin reinstates maternal ol- factory cues for nipple orientation and attachment in ratGoogle Scholar
  87. pups, Physiol. Behay. 20:385–389.Google Scholar
  88. Stevens, D., and Gerzog-Thomas, D.A., 1977, Fright reactions in rats to conspecific tissue, Physiol. Behay., 18: 47–51.CrossRefGoogle Scholar
  89. Stoddart, D.M. 1980a, “The Ecology of Vertebrate Olfaction,” Chapman and Hall, New York.Google Scholar
  90. Stoddart, D.M. 1980b, Aspects of the evolutionary biology of mammalian olfaction, in: “Olfaction in Mammals,” Zool. Soc. London, Symp., No. 45, D.M. Stoddart, ed., Academic Press, London.Google Scholar
  91. Tucker, D., and Smith, J.C., 1976, Vertebrate olfaction, in: “Evolution of Brain and Behavior in Vertebrates,” R.B. Masterson, M.E. Bitter-man, C.B.G. Campbell, and N. Hotton, eds., Lawrence Erlbaum Assoc., Hillsdale, N.J.Google Scholar
  92. Van Valen, L., 1960, Therapsids as mammals, Evolution, 14: 304–313.CrossRefGoogle Scholar
  93. Wang, R.T., and Halpern, M., 1980, Light and electron microscopic observations on the normal structure of the vomeronasal organ of garter snakes, J. Morphol., 164: 47–67.CrossRefGoogle Scholar
  94. Watson, D.M.S., 1931, On the skeleton of a Bauriamorph reptile, Proc., Zool. Soc. London., Part 3: 11–63.Google Scholar
  95. Weldon, P.J., 1980, In defense of “kairomone” as a class of chemical releasing stimuli, J. Chem. Ecol., 6: 719–725.CrossRefGoogle Scholar
  96. Weldon, P.J., 1982, The evolution of alarm pheromones, in: “Chemical Signals,” D. Müller-Schwarze, and R.M. Silverstein, eds., Plenum, New York. In press.Google Scholar
  97. Weldon, P.J. and Burghardt, G.M., 1979, The ophiophage defensiveGoogle Scholar
  98. response in crotaline snakes: Extension to new taxa, J. Chem. Ecol., 5: 141–151.Google Scholar
  99. Wilson, E.O., 1975, “Sociobiology,” Belknap/Harvard University Press, Cambridge.Google Scholar
  100. Wysocki, C.L., Wellington, J.L., and Beauchamp, G.K., 1980, Access of urinary non-volatiles to the mammalian vomeronasal organ, Science, 207: 781–783.ADSCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1983

Authors and Affiliations

  • David Duvall
    • 1
  • Michael B. King
    • 1
  • Brent M. Graves
    • 1
  1. 1.Department of Zoology and PhysiologyUniversity of WyomingLaramieUSA

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