Sexual Reprogramming and Estrogenic Sensitization in Wild Fish Exposed to Ethinylestradiol

Globally, feminization responses in wild male freshwater fish are caused by exposure to estrogenic chemicals, including natural and synthetic estrogens, contained in effluents from wastewater treatment works. In U.K. rivers, feminization responses, including intersex, are widespread in wild roach (Rutilus rutilus) populations, and severely affected fish have a reduced reproductive success. We exposed roach to environmentally relevant concentrations of the contraceptive estrogen 17 alpha-ethinylestradiol (EE2) for up to 2 years, including intermittent and repeated exposures,to determine effects on sexual development and subsequent responsiveness to estrogen. Exposure of roach to EE2 (at 4 ng/L) for 2 years resulted in sex reversal in males, leading to an all-female population with two cohorts in terms of their stages of ovarian development, one paralleling the control females and one at a significantly less advanced stage, which we propose were sex-reversed males. Differing developmental and maturing rates of the putative sex-reversed males compared with control females would question their functional capability as females in the wild. Early-life exposure to environmentally relevant concentrations of EE2 sensitized females to estrogen, as determined by the measurement of the responses of estrogen-sensitive genes in a further EE2 challenge 398 days after the original exposure. In the wild, exposure to environmentally relevant concentrations of EE2 during early life has significantly wider implications for the sexual physiology in fish than has thus far been determined.