Skip to main content
Log in

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

  • Short Communication
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Although the role of aromatase in many estrogen-dependent reproductive and metabolic functions is well documented in vertebrates, its involvement in the ovarian development of species exhibiting temperature-dependent sex determination (TSD) is incompletely understood. This is partly due to the conflicting temporal and spatial pattern of aromatase expression and activity across taxa. To help resolve this ongoing debate, we compared for the first time the embryological ontogeny of aromatase expression in turtles possessing genotypic sex determination (GSD) (Apalone mutica) and TSD (Chrysemys picta) incubated under identical conditions. As anticipated, we found no significant thermal differences in aromatase expression at any stage examined (prior to until the end of the thermosensitive period) in A. mutica. Surprisingly, the same was true for C. picta. When placed in a phylogenetic context, our results suggest that aromatase expression is evolutionarily plastic with respect to sex determination in reptiles, and that differences between reptilian TSD and GSD are not aromatase-driven. Further research across TSD and GSD species is warranted to fully decipher the evolution of functional differences among sex-determining mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

References

  • Bull JJ, Vogt RC (1981) Temperature-sensitive periods of sex determination in emydid turtles. J Exp Zool 218:435–440

    Article  PubMed  CAS  Google Scholar 

  • Desvages G, Pieau C (1992) Aromatase activity in gonads of turtle embryos as a function of the incubation temperature of eggs. J Steroid Biochem Mol Biol 41:851–853

    Article  PubMed  CAS  Google Scholar 

  • Desvages G, Girondot M, Pieau C (1993) Sensitive stages for the effects of temperature on gonadal aromatase-activity in embryos of the marine turtle dermochelys-coriacea. Gen Comp Endocrinol 92:54–61

    Article  PubMed  CAS  Google Scholar 

  • Ewert MA, Nelson CE (1991) Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1991:50–69

    Article  Google Scholar 

  • Gabriel WN, 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

    Article  PubMed  CAS  Google Scholar 

  • Janzen FJ (1993) The influence of incubation temperature and family on eggs, embryos, and hatchlings of the smooth softshell turtle (Apalone mutica). Physiol Zool 66:349–373

    Google Scholar 

  • Janzen FJ, Krenz JG (2004) Phylogenetics: which was first, TSD or GSD? In: Valenzuela N, Lance VA (eds) Temperature dependent sex determination in vertebrates. Smithsonian, Washington, DC, pp 121–130

    Google Scholar 

  • Jeyasuria P, Place AR (1998) Embryonic brain–gonadal axis in temperature-dependent sex determination of reptiles: a role for P450 aromatase (CYP19). J Exp Zool 281:428–449

    Article  PubMed  CAS  Google Scholar 

  • Murdock C, Wibbels T (2003) Cloning and expression of aromatase in a turtle with temperature dependent sex determination. Gen Comp Endocrinol 130:109–119

    Article  PubMed  CAS  Google Scholar 

  • Pieau C, Dorizzi M (2004) Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J Endocrinol 181:367–377

    Article  PubMed  CAS  Google Scholar 

  • Place AR, Lance VA (2004) The temperature-dependent sex determination drama—same cast, different stars. In: Valenzuela N, Lance VA (eds) Temperature dependent sex determination in vertebrates. Smithsonian, Washington, DC, pp 99–110

    Google Scholar 

  • Salame-Mendez A, Herrera-Munoz J, Moreno-Mendoza N, Merchant-Larios H (1998) Response of diencephalon but not the gonad to female-promoting temperature with elevated estradiol levels in the sea turtle Lepidochelys olivacea. J Exp Zool 280:304–313

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Joss JMP (1994) Steroidogenic enzyme-activity and ovarian-differentiation in the saltwater crocodile, crocodylus-porosus. Gen Comp Endocrinol 93:232–245

    Article  PubMed  CAS  Google Scholar 

  • Thomas EO, Licht P, Wibbels T, Crews D (1992) Hydroxysteroid dehydrogenase-activity associated with sexual-differentiation in embryos of the turtle Trachemys scripta. Biol Reprod 46:140–145

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela N, LeClere A, Shikano T (2006) Comparative gene expression of steroidogenic factor 1 in Chrysemys picta and Apalone mutica turtles with temperature-dependent and genotypic sex determination. Evol Dev 8:424–432

    Article  PubMed  CAS  Google Scholar 

  • van Nes S, Moe M, Andersen O (2005) Molecular characterization and expression of two cyp19 (P450 aromatase) genes in embryos, larvae, and adults of Atlantic halibut (Hippoglossus hippoglossus). Mol Rep Dev 72:437–449

    Article  Google Scholar 

  • White RB, Thomas P (1992) Adrenal–kidney and gonadal steroidogenesis during sexual differentiation of a reptile with temperature-dependent sex determination. Gen Comp Endocrinol 88:10–19

    Article  PubMed  CAS  Google Scholar 

  • 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 Endocrin 119:202–207

    CAS  Google Scholar 

  • Yntema CL (1968) A series of stages in the embryonic development of Chelydra serpentina. J Morph 125:219–252

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank D.C. Adams for critical comments on the manuscript. Eggs were collected under scientific collecting permit SC595 to N. Valenzuela from the Iowa Department of Natural Resources (DNR), as well as NH-01.0073 from the Illinois DNR, a United States Fish and Wildlife Service Special Use Permit 32576-01017, and SC 14 0001 from the Iowa DNR to F. Janzen, to whom we are very grateful. This study was funded in part by the Center for Integrative Genomics at Iowa State University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicole Valenzuela.

Additional information

Communicated by M. Hammerschmidt

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valenzuela, N., Shikano, T. 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 (2007). https://doi.org/10.1007/s00427-006-0106-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-006-0106-3

Keywords

Navigation