Is regulation of aromatase expression in reptiles the key to understanding temperature-dependent sex determination?

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 311, Issue 5, 2009, Pages 314-322

  Lance, Valentine A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REPTILIA;

AROMATASE; ESTROGEN;

ANIMAL; FEMALE; GENDER AND SEX; MALE; OVARY; PHYSIOLOGY; PRENATAL DEVELOPMENT; REPTILE; REVIEW; TEMPERATURE; TESTIS;

ANIMALS; AROMATASE; ESTROGENS; FEMALE; MALE; OVARY; REPTILES; SEX DETERMINATION (GENETICS); TEMPERATURE; TESTIS;

EID: 67649984268     PISSN: 19325223     EISSN: None     Source Type: Journal    
DOI: 10.1002/jez.465     Document Type: Article

References (72)

1. Astheimer LB, Manolis C, Grau CR. 1989. Egg formation in crocodiles: avian affinities in yolk deposition. Copeia 1989:221-224.
2. Bowden RM, Ewert MA, Nelson CE. 2002. Hormone levels in yolk decline throughout development in the red-eared slider turtle (Trachemys scripta elegans). Gen Comp Endocrinol 129:171-177.
3. Burton RF. 2002. Temperature and acid-base balance in ectothermic vertebrates: the imidazole hypotheses and beyond. J Exp Biol 205:3587-3600.
4. Carere C, Balthazart J. 2007. Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Enocrinol Metab 18:73-80.
5. Charnier M. 1966. Action de la tempe'rature sur la sex-ratio chez l'embryon d'Agama agama (Agamidae: Lacertilien). C R Se'ances Soc Biol l'Ouest Afr 160:620-622.
6. Ciofi C, Swingland IR. 1997. Environmental sex determination in reptiles. Appl Anim Sci Behav 51:251-265.
7. Conley AJ, Elf P, Corbin CJ, Dubowsky S, Fivizzani A, Lang JW. 1997. Yolk steroids decline during sexual differentiation in the alligator. Gen Comp Endocrinol 107:191-200.
8. Crews D. 1994. Temperature, steroids and sex determination. J Endocrinol 142:1-8.
9. Crews D. 1996. Temperature-dependent sex determination: the interplay of steroids hormones and temperature. Zool Sci 13:1-13.
10. Crews D, Bergeron JM. 1994. Role of reductase and aromatase in sex determination in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. J Endocrinol 143:279-289.
11. Crews D, Bergeron JM, Bull JJ, Flores D, Tousignant A, Skipper JK, Wibbels T. 1994. Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications. Dev Genet 15:297-312.
12. Crews D, Fleming A, Willingham E, Baldwin R, Skipper J. 2001. Role of steroidogenic factor 1 and aromatase in temperature-dependent sex determination in the red-eared slider turtle. J Exp Zool 290:597-606.
13. Deeming DC. 2004. Prevalence of TSD in crocodilians. In: Valenzuela N, Lance VA, editors. Temperature-dependent sex determination in vertebrates. Washington: Smithsonian Books. p 33-41.
14. Deeming DC, Ferguson MWJ. 1989. The mechanism of temperture-dependent sex determination in crocodilians: a hypothesis. Am Zool 29:973-985.
15. Desvages G, Pieau C. 1991. Steroid metabolism in gonads of turtle embryos as a function of the incubation temperature of eggs. J Steroid Biochem Mol Biol 39:203-213.
16. Dorizzi M, Mignot T-M, Guichard A, Desvages G, Pieau C. 1991. Involvement of oestrogens in sexual differentiation of gonads as a function of temperature in turtles. Differentiation 47:9-17.
17. Dorizzi M, Richard-Mercier N, Desvages G, Girondet M, Pieau C. 1994. Masculinization of gonads by aromatase inhibitors in a turtle with temperature-dependent sex determination. Differentiation 58:1-8.
18. Elf PK. 2004. Yolk steroid hormones and their possible roles in TSD species. In: Valenzuela N, Lance VA, editors. Temperature- dependent sex determination in vertebrates. Washington: Smithsonian Books. p 111-118.
19. Endo D, Park MK. 2005. Molecular cloning of P450 aromatase from the leopard gecko and its expression in the ovary. J Steroid Biochem Mol Biol 96:131-140.
20. Endo D, Kanaho Y-I, Park MK. 2008. Expression of sex steroid-related genes in the embryo of the leopard gecko. Gen Comp Endocrinol 155:70-78.
21. Ewert MA, Nelson CE. 1991. Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1991:50-69.
22. Ewert MA, Etchberger CR, Nelson CE. 2004. Turtle sexdetermining modes and TSD patterns, and some TSD pattern correlates. In: Valenzuela N, Lance VA, editors. Temperature-dependent sex determination in vertebrates. Washington: Smithsonian Books. p 21-32.
23. Freedberg S, Bowden RM, Ewert MA, Sengelaub DR, Nelson CE. 2006. Long-term sex reversal by oestradiol in amniotes with heteromorphic sex chromosomes. Biol Lett 2:378-381.
24. Gabriel W, Blumberg B, Sutton S, Place AR, Lance VA. 2001. Alligator aromatase cDNA sequence and its expression in embryos at male and female incubation temperatures. J Exp Zool 290:439-448.
25. Gardner L, Anderson T, Place AR, Dixon B, Elizur A. 2005. Sex changes strategy and the aromatase genes. J Steroid Biochem Mol Biol 94:395-404.
26. Gutie'rrez-Ospina G, Jime'nez-Trejo FJ, Favila R, Morena- Mendoza NA, Granados Ojas L, Barrios FA, DI'az-Cintra S, Merchant-Larios H. 1999. Acetylcholinstrase-positive innervation is present at undifferentiated stages of the sea turtle Lepidochelys olivacea embryo gonads: implications for temperature-dependent sex determination. J Comp Neurol 410:90-98.
27. Harlow PS. 2004. Temperature-dependent sex determination in lizards. In: Valenzuela N, Lance VA, editors. Temperature- dependent sex determination in vertebrates. Washington: Smithsonian Books. p 42-52.
28. Ho SM, Kleis S, McPherson R, Heisermann GJ, Callard IP. 1982. Regulation of vitellogenesis in reptiles. Herpetologica 38:40-50.
29. Janes DE, Bermudez D, Guillette LJ, Wayne ML. 2007. Estrogens induced male production at a female-producing temperature in a reptile (Leopard gecko, Eublepharis macularius) with temperature-dependent sex determination. J Herpetol 41:9-15.
30. Jeyasuriya P, Place AR. 1997. Temperature-dependent aromatase expression in developing diamond terrapin (Malaclemys terrapin) embryos. J Steroid Biochem Mol Biol 61:415-425.
31. Jeyasuriya P, Place AR. 1998. Embryonic brain-gonadal axis in temperature-dependent sex determination in reptiles: a role for P450 aromatase (CYP19). J Exp Zool 281:428-449.
32. Jeyasuriya P, Roosenburg WM, Place AR. 1994. Role of P-450 aromatase in sex determination of the diamondback terrapin, Malaclemys terrapin. J Exp Zool 270:95-111.
33. Johnston CM, Barnett M, Sharpe PT. 1995. The molecular biology of temperature-dependent sex determination. Philos Trans R Soc Lond B 250:297-304.
34. Lance VA. 1997. Sex determination in reptiles: an update. Am Zool 37:504-513.
35. Lance VA, Bogart MH. 1992. Disruption of ovarian development in alligator emrbyos treated with an aromatase inhibitor. Gen Comp Endocrinol 86:59-71.
36. Lang JW, Andrews HV. 1994. Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28-44.
37. Merchant-Larios H. 2001. Temperature sex determination in reptiles: the third strategy. J Reprod Dev 47:245-252.
38. Merchant-Larios H, Villalpando-Fierro I, Centeno-Urruiza B. 1989. Gonadal morphogenesis undercontrolled temperature in the sea turtle Lepidochelys olivacea. Herp Monogr 3:43-61.
39. Mitchell NJ, Nelson NJ, Cree A, Pledger S, Keall SN, Daugherty CH. 2006. Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon). Front Zool 3:1-12.
40. Morena-Mendoza N, Harley VR, Merchant-Larios H. 2001. Temperature regulates SOX9 expression in cultured gonads of Lepidochelys olivacea, a species with temperature sex determination. Dev Biol 229:319-326.
41. Mrosovsky N, Pieau C. 1991. Transitional range of temperature, pivotal temperatures and thermosensistive stages for sex determination in reptiles. Amphibia-Reptilia 12: 169-179.
42. Murdock C, Wibbels T. 2003. Cloning and expression of aromatase in a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 130:109-119.
43. O'Steen S. 1998. Embryonic temperature influences juvenile temperature choice and growth rate in snapping turtles Chelydra serpentina. J Exp Biol 201:439-449.
44. Pieau C. 1996. Temperature variation and sex determination in reptiles. Bioessays 18:19-26.
45. Pieau C, Dorizzi M. 2004. Oestrogens and temperaturedependent sex determination in reptiles: all is in the gonads. J Endocrinol 181:367-377.
46. Pieau C, Dorizzi M, Richard-Mercier N. 1999. Temperaturedependent sex determination and gonadal differentiation in reptiles. Cell Mol life Sci 55:887-900.
47. Pieau C, Dorizzi M, Richard-Mercier N. 2001. Temperaturedependent sex determination and gonadal differentiation in reptiles. In: Scherer G, Schmid M, editors. Genes and mechanisms in vertebrate sex determination. Basel: Birkha ̈user, Verlag. p 117-141.
48. Place AR, Lance VA. 2004. The temperature-dependent sex determination drama: same cast different stars. In: Valenzuela N, Lance VA, editors. Temperature-dependent sex determination in vertebrates. Washington: Smithsonian Books. p 99-110.
49. Place AR, Lang J, Gavasso S, Jeyasuriya P. 2001. Expression of P450arom in Malaclemys terrapin and Chelydra serpentina: a tale of two sites. J Exp Zool 290:673-690.
50. Quinn AE, Georges A, Sarre SD, Guarino, F, Ezaz T, Marshall Graves J. 2007. Temperature sex reversal implies gene dosage in a reptile. Science 316:411.
51. Radder RS. 2007. Maternally derived egg yolk steroid hormones and sex determination: review of a paradox in reptiles. J Biosci 32:1213-1220.
52. Radder R, Ali S, Shine R. 2007. Offspring sex is not related to maternal allocation of yolk steroids in the lizard Bassiana duperreyi (Scincidae). Physiol Biochem Zool 80:220-227.
53. Ramsey M, Crews D. 2007. Adrenal-kidney-gonad complex measurements may not predict gonad-specific changes in gene expression patterns during temperature-dependent sex determination in the red-eared slider turtle (Trachemys scripta elegans). J Exp Zool 307A:463-470.
54. Ramsey M, Shoemaker C, Crews D. 2007. Gonadal expression of Sf1 and aromatase during sex determination in the redeared slider turtle (Trachemys scripta), a reptile with temperature-dependent sex determination. Differentiation 78:978-991.
55. Raynaud A, Pieau C. 1985. Embryonic development of the genital system. In: Gans C, Billett F, editors. Biology of the reptilia, development B, Vol. 15. New York: Wiley-Interscience. p 149-299.
56. Rhen T, Lang JW. 1995. Phenotypic plasticity for growth in the common snapping turtle: effects of incubation temperature, clutch, and their interaction. Am Nat 146:726-747.
57. Rhen T, Metzger K, SAchroeder A, Woodward R. 2007. Expression of putative sex-determining genes during the thermosensitive period of gonadal development in the snapping turtle, Chelydra serpentina. Sex Dev 1:255-270.
58. Salame-Mendez A, Herrera-Munoz J, Morena-Mendoza N, Merchant-Larios H. 1998. Response of diencephalons but not gonad to female-promoting temperature with elevated estradiol levels in the sea turtle Lepidochelys olivacea. J Exp Zool 280:304-313.
59. Sarre SD, Georges A, Quinn A. 2004. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26:639-645.
60. Shine R, Elphick MJ, Donnellan S. 2002. Co-occurrence of multiple, supposedly incompatible modes of sex determination in a lizard population. Ecol Lett 5:486-489.
61. Shoemaker CM, Queen J, Crews D. 2007a. Response of candidate sex determining genes to changes in temperature reveals their involvement in the molecular network underlying temperature-dependent sex determination. Mol Endocrinol 21:2750-2763.
62. Shoemaker CM, Ramsey M, Queen J, Crews D. 2007b. Expression of Sox9, Mis, and Dmrt1 in the gonad of a species with temperature-dependent sex determination. Dev Dyn 236:1055-1063.
63. Smith AMA. 1987. The sex and survivorship of embryos and hatchlings of the Australian freshwater crocodile, Crocodylus johnstoni. Ph.D. Thesis. School of Botany and Zoology, Australian National University, Canberra, Australia.
64. Smith CA, Joss JMP. 1994. Steroidogenic enzyme activity and ovarian differentiation in the Saltwater crocodile, Crocodylus porosus. Gen Comp Endocrinol 93:232-245.
65. Smith CA, Elf PK, Lang JW, Joss JMP. 1995. Aromatase activity during gonadal sex differentiation in alligator embryos. Differentiation 58:281-290.
66. Torres Maldonado LC, Landa Piedra A, Moreno Mendoza N, Marmolejo Valencia A, Meza MartI'nez A, Merchant-Larios H. 2002. Expression profiles of Dax1, Dmrt1, and Sox9 during temperature sex determination in gonads of the sea turtle Lepidochelys olivacea. Gen Comp Endocrinol 129:20-26.
67. Valenzuela N, Shikano T. 2007. Embryological ontogeny of aromatase gene expression in Chrysemys picta and Apalone mutica turtles: comparative patterns within and across temperature-dependent and genotypic sex determining mechanisms. Dev Genes Evol 217:55-62.
68. Webb GJW, Manolis SC, Preston-Cooper H. 1990. Crocodile management and research in the Northern Territory 1988-1990. In: Proceedings of the 10th Working Meeting of the Crocodile Specialist Group, IUCN-World Conservation Union, Gainesville, Florida, p 253-273.
69. Wibbels T, Crews D. 1994. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J Endocrinol 141:295-299.
70. Wibbels T, Bull JJ, Crews D. 1991. Synergism between temperature and estradiol: a common pathway in turtle sex determination? J Exp Zool 260:130-134.
71. Willingham E, Baldwin R, Skipper JK, Crews D. 2000. Aromatase activity during embryogenesis in the brain and adrenal-kidney-gonad of the red-eared slider turtle, a species with temperature-dependent sex determination. Gen Comp Endocrinol 199:202-207.
72. Yao HH-C, Capel B. 2005. Temperature, genes, and sex: a comparative view of sex determination in Trachemys scripta and Mus musculus. J Biochem 138.