Get access

An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish, Danio rerio

Authors

  • Martina Fenske,

    Corresponding author
    1. Department of Chemical Ecotoxicology, UFZ Centre for Environmental Research, 04318 Leipzig, Germany
    Current affiliation:
    1. M. Fenske is Environmental and Molecular Fish Biology EMFB, Hatherly Laboratories, University of Exeter, Prince of Wales Road, Exeter EX4 4PS, United Kingdom
    • Department of Chemical Ecotoxicology, UFZ Centre for Environmental Research, 04318 Leipzig, Germany
    Search for more papers by this author
  • Gerd Maack,

    1. Department of Chemical Ecotoxicology, UFZ Centre for Environmental Research, 04318 Leipzig, Germany
    Search for more papers by this author
  • Christoph Schäfers,

    1. Institute for Molecular Biology and Applied Ecology IME, 57392 Schmallenberg, Germany
    Search for more papers by this author
  • Helmut Segner

    1. Centre for Fish and Wildlife Health, University of Bern, CH-3012 Bern, Switzerland
    Search for more papers by this author

Abstract

The aim of the present study was to elucidate how full life-cycle exposure to estrogens impacts zebrafish development and reproduction, compared to partial life-cycle exposure only, and whether the estrogen-induced effects in zebrafish are reversible or irreversible. Zebrafish were exposed in a flow-through system to an environmentally relevant concentration (3 ng/L) of the synthetic estrogen 17α-ethinylestradiol (EE2) either from fertilization until the all-ovary stage of gonad development (i.e., 42 d postfertilization [DPF] in our experiment) or from fertilization until the reproductive stage (i.e., 118 DPF). Reversibility of the estrogen-induced effects was assessed after 58 d of depuration in EE2-free water until 176 DPF. Early life exposure led to a lasting induction of plasma vitellogenin (VTG) in adult females but altered neither the sex ratio nor the reproductive capabilities. Full life-cycle exposure resulted in elevated VTG concentrations and caused gonadal feminization in 100% of exposed fish and thus inhibited reproduction. Two types of ovaries were observed in continuously exposed adult fish, immature ovaries with primary growth stage oocytes only and mature ovaries containing the full range of all oocyte maturation stages. Fish with immature ovaries had plasma VTG levels like control males, while fish with mature ovaries had female-like VTG levels. The effects of full life cycle exposure were at least partly reversible, and 26% of fish of the previous all-female cohort developed fully differentiated testes. These findings suggest that continuous estrogen exposure had arrested the developmental transition of the gonads of genetic males from the early all-ovary stage to functional testes. After the exposure had ceased, however, these males apparently were able to accomplish testicular differentiation.

Ancillary