Sex differences in the nervous system of reptiles

Cellular and Molecular Neurobiology

Volumn 17, Issue 6, 1997, Pages 649-669

  Godwin, John ^a,b   Crews, David ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

2 deoxyglucose; Cytochrome oxidase; Hypothalamus; Preoptic; Receptors; Reptiles; Sexual behavior; Sexual differentiation; Steroid hormones

Indexed keywords

SEX HORMONE; STEROID HORMONE; STEROID RECEPTOR;

ARTICLE; FEMALE; FOREBRAIN; LIMBIC SYSTEM; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REPTILE; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR;

ANIMALS; BRAIN; FEMALE; MALE; REPTILES; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

EID: 0031473335     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022586003789     Document Type: Article

References (83)

1. Allen, E., and Crews, D. (1992). Male sexual behavior and 2-deoxyglucose uptake in the red-sided garter snake (Thamnophis sirtalis parietalis). Brain Behav. Evol. 40:17-24.
2. Bass, A. H. (1992). Dimorphic male brains and alternative reproductive tactics in a vocalizing fish. Tr. Neurosci. 15:139-145.
3. Blaustein, J. D., and Turcotte, J. C. (1990). Down-regulation of progestin receptors in guinea pig brain: New findings using an immunocytochemical technique. J. Neurosci. 21:675-685.
4. Brown, T. J., and MacLusky, N. J. (1994). Progesterone modulation of estrogen receptors in microdissected regions of the rat hypothalamus. Mol. Cell. Neurosci. 5:283-290.
5. Bull, J. J. (1983). Evolution of Sex Determining Mechanisms, Benjamin/Cummings, Menlo Park.
6. Burger, J. (1989). Incubation temperature has long-term effects on behaviour of young pine snakes (Pituophis melanoleucus). Behav. Ecol. Sociobiol. 24:201-207.
7. Burger, J. (1990). Effects of incubation temperature on behavior of young Black Racers (Coluber constrictor) and Kingsnakes (Lampropeltis getulus). J. Herpetol. 24:158-163.
8. Coomber, P., Gonzalez-Lima, F., and Crews, D. (1997). Effects of incubation temperature and gonadal sex on the morphology and metabolic capacity of brain nuclei in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. J. Comp. Neurology 380:409-421.
9. Cooper, W. E., Jr., and Greenberg, N. (1992). Reptilian coloration and behavior. In Gans, C., and Crews, D. (eds.), Biology of the Reptilia, Vol. 18 Physiology E. Hormones, Brain and Behavior, University of Chacago Press, Chicago, pp. 298-422.
10. Craig, A. D., Bushnell, M, C., Zhang, E.-T., and Blomqvist, A. (1994). A thalamic nucleus specific for pain and temperature sensation. Nature 372:770-773.
11. Crews, D. (1985). Effects of early sex hormone treatment on courtship behavior and sexual attractivity in the red-sided garter snake, Thamnophis sirtalis parietalis. Physiol. Behav. 35:569-575.
12. Crews, D. (1988). The problem with gender. Psychobiology 16: 321-334.
13. Crews. D. (1989). Unisexual organisms as model systems for research in the behavioral neurosciences. In Dawley, R. M., and Bogart, J. P. (eds.), Evolution and Ecology of Unisexual Vertebrates, New York State Museum, Albany, pp. 132-143.
14. Crews, D. (1991). Trans-seasonal action of androgen in the control of spring courtship behavior in male red-sided garter snakes. Proc. Natl. Acad. Sci. USA 88:3545-3548.
15. Crews, D. (1996). Temperature-dependent sex determination: The interplay of steroid hormones and temperature. Zool. Sci. 6:1-12.
16. Crews, D., and Bull, J. J. (1987). Evolutionary insights from reptilian sexual differentiation. In Haseltine, F. P., McClure, M. E., and Goldberg, E. H. (eds.), Genetic Markers of Sexual Differentiation, Plenum Press, New York, pp. 11-26.
17. Crews, D., and Fitzgerald, K. T. (1980). "Sexual" behavior in parthenogenetic lizards (Cnemidophorus). Proc. Natl. Acad. Sci. USA 77:499-502.
18. Crews, D., and Gans, C. (1992). The interaction of hormones, brain, and behavior. An emerging discipline in herpetology. In Gans, C., and Crews, D. (eds.), Biology of the Reptilia, Vol. 18, Physiology E. Hormones, Brain and Behavior, University of Chicago Press, Chicago, pp. 1-23.
19. Crews, D., and Moore, M. C. (1993). Psychobiology of reproduction of parthenogenetic whiptail lizards. In Wright, J. W., and Vitt, L. J. (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), Herpetologist's League Special Publication No. 3, Oklahoma Museum of Natural History, Norman, pp. 257-282.
20. Crews, D., Camazine, B., Diamond, M., Mason, R., Tokarz, R. R., and Garstka, R. (1984). Hormonal independence of courtship behavior in the male garter snake. Horm. Behav. 18: 29-41.
21. Crews, D., Wade, J., and Wilczynski, W. (1990). Sexually dimorphic areas in the brain of whiptail lizards. Brain Behav. Evol. 36:262-270.
22. Crews, D., Robker, R., and Mendonça, M. (1993). Seasonal fluctuations in brain nuclei in the red-sided garter snake and their hormonal control. J. Neurosci. 13:5356-5364. "red-sided garter snake and their hormonal control. J. Neurosci. 13:5356-5364.
23. Davis, M. R., and Fernald, R. D. (1990). Social control of neuronal soma size. J. Neurobiol. 21:1180-1188.
24. Flores, D., and Crews, D. (1995). Effect of hormonal manipulation on sociosexual behavior in adult female leopard geckos (Eublepharis macularius), a species with temperature-dependent sex determination. Horm. Behav. 29: 458-473.
25. Flores, D., Tousignant, A., and Crews, D. (1994). Incubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius). Physiol. Behav. 55:1067-1072.
26. Francis, R. C., Soma, K., and Fernald, R. D. (1993). Social regulation of the brain-pituitary-gonadal axis. Proc. Natl. Acad. Sci. USA 90:7794-7798.
27. Godwin, J., and Crews, D. (1995). Sex differences in estrogen and progesterone receptor messenger ribonucleic acid regulation in the brain of little striped whiptail lizards. Neuroendocrinlogy 62:293-300.
28. Godwin, J., Hartman, V., Grammer, M., and Crews, D. (1996). Progesterone inhibits female-typical receptive behavior and decreases hypothalamic estrogen and progesterone receptor messenger ribonucleic acid levels in whiptail lizards (genus Cnemidophorus). Horm. Behav. 30:138-144.
29. Gonzalez-Lima, F. (1992). Brain imaging of auditory learning functions in rats: studies with fluorodeoxyglucose autoradiography and cytochrome oxidase histochemistry. In Gonzalez-Lima, F., Finkenstadt, T., and Scheich, H. (eds). Advances in Metabolic Mapping Techniques for Brain Imaging of Behavioral and Learning Functions, NATO ASI Series D68, Kluwer Academic, Boston, pp. 39-109.
30. Gorski, R. A. (1984). Critical role for the medial preoptic area in the sexual differentiation of the brain. In De Vries, C. J., De Bruin, J. P. C., Uylings, H. B. M., and Corner, M. A. (eds.), Progress in Brain Research, Elsevier, New York, Oxford, Vol. 61, p. 129.
31. Grassman, M., and Crews, D. (1986). Progesterone induction of pseudocopulatory behavior and stimulus-response complementarity in an all-female lizard species. Horm. Behav. 20: 327-335.
32. Greenberg, N. (1977). Ethological considerations in the experimental study of lizard behavior. In Greenberg, N., and MacLean, P. D. (eds.), Behavior and Neurology of Lizards, NIMH, Rockville, MD, pp. 203-224.
33. Grober, M. S., and Bass, A. H. (1991). Neuronal correlates of sex/role change in labrid fishes: LHRH-like immunoreactivity. Brain Behav. Evol. 38:302-312.
34. Grober, M. S., Jackson, I. M. D., and Bass, A. H. (1991). Gonadal steroids affect LHRH preoptic cell number in a sex/role changing fish. J. Neurobiol. 22:734-741.
35. Grober, M. S., Fox, S. H., Laughlin, C., and Bass, A. H. (1994). GnRH cell size and number in a teleost fish with two male reproductive morphs: Sexual maturation, final sexual status and body size allometry. Brain Behav. Evol. 43:61-78.
36. Goy, R. W., and McEwen, B. S. (1980). Sexual Differentiation of the Brain, MIT Press, Cambridge.
37. Hews, D. K., and Moore, M. C. (1996). A critical period for the organization of alternative male phenotypes of tree lizards by exogenous testosterone? Physlol. Behav. 60:425-429.
38. Hews, D. K., Knapp, R., and Moore, M. C. (1994). Early exposure to androgens affects adult expression of alternative male types of tree lizards. Horm. Behav. 28:96-115.
39. Hover, E. L. (1985). Differences in aggressive behavior between two throat color morphs in a lizard, Urosaurus ornatus. Copeia 1985:933-940.
40. Jones, D., Gonzalez-Lima, F., Crews, D., Galef, B. G., and Clark, M. M. (1994). Effects of intrauterine position on metabolic capacity of the hypothalamus in the gerbil: a cytochrome oxidase study. Soc. Neurosci. Abstr. 20:1739 (abstr. 709.6).
41. Jones, D., Gonzalez-Lima, F., Crews, D., Galef, B. G., and Clark, M. M. (1997). Effects of intrauterine position on hypothalamic activity of female gerbils: A cytochrome oxidase histochemistry study. Physiol. Behav. 61:513-519.
42. Kendrick, A. M., Rand, M. S., and Crews, D. (1995). Electrolytic lesions of the ventromedial hypothalamus abolish sexual receptivity in female whiptail lizards, Cnemidophorus uniparens. Brain Res. 680:226-228.
43. Kingston, P. A., and Crews, D. (1994). Role of the AH-POA in the control of courtship and copulatory behavior in sexual and unisexual whiptail lizards. Brain Res. 643:349-351.
44. Knapp, R., and Moore, M. C. (1995). Hormonal responses to aggression vary with type of agonistic encounter in tree lizards, Urosaurus ornatus. Horm, Behav. 29:85-105
45. Knapp, R., and Moore, M. C. (1996). Alternative male morphs in tree lizards (Urosaurus ornatus) have different delayed hormonal responses to aggressive encounters. Anim. Behav. 52:1045-1055.
46. Lank, D. B., Smith, C. M., Hanotte, O., Burke, T., and Cooke, F. (1995). Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62.
47. Marler, C. A., Wilczynski, W., and Gonzalez-Lima, F. (1992). Metabolic mapping using cytochrome oxidase histochemistry in frog brain areas associated with auditory processing and reproductive behavior. Soc. Neurosci. Abstr. 18:367.3.
48. Mason, R. T. (1992). Reptile pheromones. In Gans, C., and Crews, D. (eds.), Biology of the Reptilia, Vol. 18, Physiology E. Hormones, Brain and Behavior, University of Chacago Press, Chicago, pp. 114-228.
49. Mason, R. T., and Crews, D. (1985). Female mimicry in garter snakes. Nature 316:59-60.
50. 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.
51. Mendonca, 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.
52. Mendonca, M. T., Daniels, D., Faro, C., and Crews, D. (1996). Receptivity and 2-deoxyglucose uptake in female red-sided garter snakes (submitted for publication).
53. Moore, M. C. (1991). Application of organization-activation theory to alternative male reproductive strategies: A review. Horm. Behav. 25:154-179.
54. Moore, M. C., and Crews, D. (1986). Sex steroid hormones in natural populations of a sexual whiptail lizard, Cnemidophorus inornatus, a direct evolutionary ancestor of a unisexual parthenogen. Gen. Comp. Endocrinol. 63:424-430.
55. Moore, M. C., and Lindzey, J. (1992). Physiological bases of sexual and territorial behavior in male reptiles. In Gans, C., and Crews, D. (eds.), Biology of the Reptilia, Vol. 18, Physiology E. Hormones, Brain and Behavior, University of Chicago Press, Chicago, pp. 70-113.
56. Moore, M. C., Whittier, J. M., and Crews, D. (1985). Sex steroid hormones during the ovarian cycle of an all-female, parthenogenetic lizard and their correlation with pseudosexual behavior. Gen. Comp. Endocrinol. 60:144-153.
57. Nottebohm, F. (1989). Hormonal regulation of synapses and cell number in adult canary brain and its relevance to theories of long-term memory storage. In Lakoskin, J. M. Perez-Plo, J. R., and Rassin, D. K. (eds.), Neural Control of Reproductive Function, Alan R. Liss, New York, pp. 583-601.
58. Panzica, G. C., Viglietti-Panzica, C., Calacagni, M., Anselmetti, G. C., Schumacher, M., and Balthazart, J. (1987). Sexual differentiation and hormonal control of the sexually dimorphic medial preoptic nucleus in the quail. Br. Res. 416:59-68.
59. Pfaff, D. W., Schwartz-Giblin, S., McCarthy, M. M., and Kow, L-M. (1994) Cellular and molecular mechanisms of female reproductive behaviors. In Neill, J. D., and Knobil, E. (eds.), The Physiology of Reproduction, vol. 2, Raven Press, New York, pp. 107-220.
60. Popper, C. R., Jones, R. E., and Lopez, K. H. (1992). Distribution of arginine vasotocin in the brain of the lizard Anolis carolinensis, Cell Tissue Res. 267:391-398.
61. Rand, M. S. (1991). Behavioral Function and Hormonal Control of Polymorphic Sexual Coloration in the Lizard Sceloporus undulatus erythrocheilus. Doctoral Dissertation, University of Colorado, Boulder.
62. Rand, M. S. (1992). Hormonal control of polymorphic and sexually dimorphic coloration in the lizard Sceloporus undulatus erythrocheilus. Gen. Comp. Endocrinol. 88:461-468.
63. Rand, M. S., and Crews, D. (1994). The bisexual brain: Sex differences and sex behaviour differences in sexual and parthenogenetic lizards. Brain Res. 665:163-167.
64. Satinoff, E. (1983). A reevaluation of the concept of the homeostatic organization of temperature regulation. In Satinoff, E., and Teitlebaum, P. (eds.), Handbook of Behavioral Neurobiology, Vol. 6. Motivation., Plenum Press, New York, pp. 483-472.
65. Shine, R., and Crews, D. (1988). Why male garter snakes have small heads: The evolution and endocrine control of sexual dimorphism. Evolution 42: 1105-1110.
66. Smeets, W. J., Sevensma, J. J., and Jonker, A. J. (1990). Comparative analysis of vasotocin-like immunoreactivity in the brain of the turtle Pseudemys scripta elegans and the snake Python regius. Brain Behav. Evol. 35:65-84.
67. Stoll, C. J., and Voorn, P. (1981). The distribution of hypothalamic and extrahypothalamic vasotocinergic cells and fibers in the brain of a lizard, Gekko geckko: Presence of a sex difference. J. Comp. Neurol. 239:193-204.
68. Thepen, Th., Voorn, P., Stoll, D. J., Sluiter, A. A., Pool, C. W., and Lohman, A. H. M. (1987). Mesotocin and vasotocin in the brain of the lizard Gekko gecko: An immunocytochemical study. Cell Tissue Res. 250: 649-656.
69. Thompson, C. W., and Moore, M. C. (1991). Syntopic occurrence of multiple dewlap color morphs in male tree lizards, Urosaurus ornatus. Copeia 1991:493-503.
70. Thompson, C. W., and Moore, M. C. (1992). Behavioral and hormone correlates of alternative reproductive strategies in a polygynous lizard: Tests of the relative plasticity and challenge hypotheses. Horm. Behav. 26:568-585.
71. Wade, J., and Crews, D. (1991). The relationship between reproductive state and "sexually" dimorphic brain areas in sexually reproducing and parthenogenetic whiptail lizards. J. Comp. Neurol., 309:507-514.
72. Wade, J., and Crews, D. (1992). Sexual dimorphisms in the soma size of neurons in the brain of whiptail lizards (Cnemidophorus species). Brain Res. 594:311-314.
73. Wade, J., Huang, J-M., and Crews, D. (1993). Hormonal control of sex differences in the brain, behavior, and accessory sex structures of whiptail lizards (Cnemidophorus species). J. Neuroendocrinol. 5:81-93.
74. Wennstrom, K. L., and Crews, D. (1995). Making males from females: The effects of aromatase inhibitors on a parthenogenetic species of whiptail lizard. Gen. Comp. Endocrinol. 99:316-322.
75. Whittier, J., and Tokarz, R. R. (1992). Physiological bases of sexual receptivity in female reptiles. In Gans, C., and Crews, D. (eds.), Biology of the Reptilia: Vol. 18, Physiology E. Hormones, Brain and Behavior, University of Chicago Press, Chicago, pp. 24-69.
76. Wibbels, T., and Crews, D. (1994). Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with TSD. J. Endocrinol. 141:295-299.
77. Wright, J. W. (1993). Evolution of the lizards of the genus Cnemidophorus. In Wright, J. W., and Vitt, L. J. (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), Herpetologist's League Special Publication No. 3, Oklahoma Museum of Natural History, Norman, pp. 27-82.
78. Yahr, P. (1995). Neural circuitry for the hormonal control of male sexual behavior. In Micevych, P. E., and Hammer, R. P. (eds.), Neurobiological Effects of Sex Steroid Hormones., Cambridge University Press, Cambridge, England, pp. 40-56.
79. Young, L. J., and Crews, D. (1995). Comparative neuroendocrinology of steroid receptor gene expression and regulation: Relationship to physiology and behavior. Tr. Endocrinol. Metabol. 6:317-323.
80. Young, L. J., Lopreato, G. F., Horan, K., and Crews, D. (1994). Cloning and in situ hybridization of estrogen receptor, progesterone receptor, and androgen receptor expression in the brain of whiptail lizards (Cnemidophorus uniparens and C. inornatus). J. Comp. Neurol. 347:288-300.
81. Young, L. J., Nag, P. K., and Crews, D. (1995a). Species differences in behavioral and neural sensitivity to estrogen in whiptail lizards: Correlation with hormone receptor messenger ribonucleic acid expression. Neuroendocrinology 61:680-686.
82. Young, L. J., Nag, P. K., and Crews, D. (1995b). Regulation of estrogen and progesterone receptor messenger ribonucleic acid by estrogen in the brain of the whiptail lizard (Cnemidophorus uniparens). J. Neuroendocrinol. 7:119-125.
83. Young, L. J., Nag, P. K., and Crews, D. (1995c). Species differences in estrogen receptor and progesterone receptor mRNA expression in the brain of sexual and unisexual lizards. J. Neuroendocrinol. 7:567-576.