Abstract
This study aimed to investigate the male-to-female morphological and physiological transdifferentiation process in rainbow trout (Oncorhynchus mykiss) exposed to exogenous estrogens. The first objective was to elucidate whether trout develop intersex gonads under exposure to low levels of estrogen. To this end, the gonads of an all-male population of fry exposed chronically (from 60 to 136 days post fertilization – dpf) to several doses (from environmentally relevant 0.01 µg/L to supra-environmental levels: 0.1, 1 and 10 µg/L) of the potent synthetic estrogen ethynylestradiol (EE2) were examined histologically. The morphological evaluations were underpinned by the analysis of gonad steroid (testosterone, estradiol and 11-ketotestosterone) levels and of brain and gonad gene expression, including estrogen-responsive genes and genes involved in sex differentiation in (gonads: cyp19a1a, ER isoforms, vtg, dmrt1, sox9a2; sdY; cyp11b; brain: cyp19a1b, ER isoforms). Intersex gonads were observed from the first concentration used (0.01 µg EE2/L) and sexual inversion could be detected from 0.1 µg EE2/L. This was accompanied by a linear decrease in 11-KT levels, whereas no effect on E2 and T levels was observed. Q-PCR results from the gonads showed downregulation of testicular markers (dmrt1, sox9a2; sdY; cyp11b) with increasing EE2 exposure concentrations, and upregulation of the female vtg gene. No evidence was found for a direct involvement of aromatase in the sex conversion process. The results from this study provide evidence that gonads of male trout respond to estrogen exposure by intersex formation and, with increasing concentration, by morphological and physiological conversion to phenotypic ovaries. However, supra-environmental estrogen concentrations are needed to induce these changes.
Highlights
Gonads are unique among all organs given their bipotential nature: they can develop either into an ovary or a testis from a single primordium
Though these pathways are still not well understood in mammals, the situation is even more complex in fish, since they display a great variety of sex determination systems, and because sex differentiation can be subject to exogenous influences, which can override the presumptive developmental route [2]
We focus on key genes of the steroidogenesis, with cyp11b2.1, the gene encoding the enzyme 11b-hydroxylase involved in the 11-oxygenated androgen production; and the gonads and brain isoforms of the aromatase, the enzyme which synthesizes estradiol
Summary
Gonads are unique among all organs given their bipotential nature: they can develop either into an ovary or a testis from a single primordium. The germinal epithelium is composed of germ cells which develop into sperm or eggs and somatic cells, involved in gamete maturation, which differentiate into Sertoli or follicular cells, depending on the destiny of the gonad This leads to a plasticity of this developmental pathway. The way by which cells choose between either fate is genetically controlled by the expression of a main male gene SRY that leads irrefutably to testis development [1] Though these pathways are still not well understood in mammals, the situation is even more complex in fish, since they display a great variety of sex determination systems, and because sex differentiation can be subject to exogenous influences, which can override the presumptive developmental route (i.e. temperature in zebrafish) [2]. Given that one mating type can be more marketable, this practice is commonly used in fish farming to obtain unisexual populations [4,5,6]
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