Abstract
Complete sex reversal of fish is accomplished routinely in aquaculture practices by exposing fish to exogenous sex steroids during gonadal differentiation. A variety of environmental chemicals are also active at sex steroid receptors and theoretically possess the potential to alter normal sexual differentiation in fish. However, in controlled environmental chemical exposures to date, only partial alterations of fish sexual phenotype have been observed. Here we report complete, permanent, and functional male-to-female sex reversal in the Japanese medaka (Oryzias latipes, d-rR strain) after a onetime embryonic exposure to the xenoestrogen o, p'-DDT. d-rR strain medaka are strict gonochorists that possesses both sex-linked pigmentation, which distinguishes genotypic sex, and sexually dimorphic external secondary sexual characteristics, which distinguish phenotypic sex. We directly microinjected the xenoestrogen o, p'-DDT into the egg yolks of medaka at fertilization to parallel the maternal transfer of lipophilic contaminants to the embryo. At 10 weeks of age, microinjected medaka were examined for mortality and sex reversal. A calculated embryonic dose of 511 +/- 22 ng/egg o, p'-DDT (mean +/- standard error) resulted in 50% mortality. An embryonic exposure of 227 +/- 22 ng/egg o, p'-DDT resulted in 86% (6 of 7) sex reversal of genetic males to a female phenotype (XY females). XY females were distinguished by sex-linked male pigmentation accompanying female secondary sexual characteristics. Histologic examination of the gonads confirmed active ovaries in 100% of the XY females. In 10-day breeding trials in which XY females were paired with normal XY males, 50% of the XY females produced fertilized embryos; this represents a comparable breeding success rate to normal XX females. Fertilized eggs produced from XY females hatched to viable larvae. These results clearly indicate that a weakly estrogenic pesticide, o, p'-DDT, when presented during the critical period of gonadal development, can profoundly alter sexual differentiation.
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- Aida T. On the Inheritance of Color in a Fresh-Water Fish, APLOCHEILUS LATIPES Temmick and Schlegel, with Special Reference to Sex-Linked Inheritance. Genetics. 1921 Nov;6(6):554–573. doi: 10.1093/genetics/6.6.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bitman J., Cecil H. C., Harris S. J., Fries G. F. Estrogenic activity of o,p'-DDT in the mammalian uterus and avian oviduct. Science. 1968 Oct 18;162(3851):371–372. doi: 10.1126/science.162.3851.371. [DOI] [PubMed] [Google Scholar]
- Edmunds J. S., Fairey E. R., Ramsdell J. S. A rapid and sensitive high throughput reporter gene assay for estrogenic effects of environmental contaminants. Neurotoxicology. 1997;18(2):525–532. [PubMed] [Google Scholar]
- Edmunds J. S., McCarthy R. A., Ramsdell J. S. Ciguatoxin reduces larval survivability in finfish. Toxicon. 1999 Dec;37(12):1827–1832. doi: 10.1016/s0041-0101(99)00119-1. [DOI] [PubMed] [Google Scholar]
- Folmar L. C., Denslow N. D., Rao V., Chow M., Crain D. A., Enblom J., Marcino J., Guillette L. J., Jr Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect. 1996 Oct;104(10):1096–1101. doi: 10.1289/ehp.961041096. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gellert R. J., Heinrichs W. L., Swerdloff R. S. DDT homologues: estrogen-like effects on the vagina, uterus and pituitary of the rat. Endocrinology. 1972 Oct;91(4):1095–1100. doi: 10.1210/endo-91-4-1095. [DOI] [PubMed] [Google Scholar]
- Nelson J. A. Effects of dichlorodiphenyltrichloroethane (DDT) analogs and polychlorinated biphenyl (PCB) mixtures on 17beta-(3H)estradiol binding to rat uterine receptor. Biochem Pharmacol. 1974 Jan 15;23(2):447–451. doi: 10.1016/0006-2952(74)90436-5. [DOI] [PubMed] [Google Scholar]
- Nimrod A. C., Benson W. H. Xenobiotic interaction with and alteration of channel catfish estrogen receptor. Toxicol Appl Pharmacol. 1997 Dec;147(2):381–390. doi: 10.1006/taap.1997.8296. [DOI] [PubMed] [Google Scholar]
- Robison A. K., Schmidt W. A., Stancel G. M. Estrogenic activity of DDT: estrogen-receptor profiles and the responses of individual uterine cell types following o,p'-DDT administration. J Toxicol Environ Health. 1985;16(3-4):493–508. doi: 10.1080/15287398509530758. [DOI] [PubMed] [Google Scholar]
- Strandberg B., Strandberg L., van Bavel B., Bergqvist P. A., Broman D., Falandysz J., Näf C., Papakosta O., Rolff C., Rappe C. Concentrations and spatial variations of cyclodienes and other organochlorines in herring and perch from the Baltic Sea. Sci Total Environ. 1998 Apr 23;215(1-2):69–83. doi: 10.1016/s0048-9697(98)00114-4. [DOI] [PubMed] [Google Scholar]
- Sumpter J. P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect. 1995 Oct;103 (Suppl 7):173–178. doi: 10.1289/ehp.95103s7173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- White R., Jobling S., Hoare S. A., Sumpter J. P., Parker M. G. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology. 1994 Jul;135(1):175–182. doi: 10.1210/endo.135.1.8013351. [DOI] [PubMed] [Google Scholar]
- YAMAMOTO T. Artificial induction of functional sex-reversal in genotypic females of the medaka (Oryzias latipes). J Exp Zool. 1958 Mar;137(2):227–263. doi: 10.1002/jez.1401370203. [DOI] [PubMed] [Google Scholar]





