Environmental Estrogen-Induced Alterations of Male Aggression and Dominance Hierarchies in Fish: A Mechanistic Analysis

Environmental estrogens have been shown to affect aspects of fish behavior that could potentially impact on wild populations, but the physiological mechanisms underpinning these effects are unknown. Using small colonies of zebrafish (Danio rerio), we evaluated the impacts of estrogen exposure on the aggression of dominant males, the associated implications for their social status and reproductive success, and their signaling mechanisms. The aggression of dominant males exposed to 17α-ethinylestradiol (EE2; 10 ng/L nominal) was reduced significantly, and half of these fish subsequently lost their dominance, behavioral changes that were reflected in their reproductive success. Plasma androgen and the expression of genes involved in sex steroid production/signaling (cyp19a1b, cyp17, hsd11b2, hsd17b3, ar) and aggression (avplrv1b, tph1b, htr1a, sst1, sstr1, th, slc6a3, ar) were higher in control dominant versus subordinate males, but suppressed by EE2 exposure, such that the differences between the social ranks were not retained. The expression levels of avpl (brain), which promotes aggression and dominance, and ar and cyp17 (gonad) were elevated in nonexposed males paired with EE2-exposed males. Our findings illustrate that disruptions of behaviors affecting social hierarchy, and in turn breeding outcome, as a consequence of exposure to an environmental estrogen are signaled through complex interconnecting gonadal and neurological control mechanisms that generally conform with those established in mammalian models. The extensive molecular, genetic, physiological, and behavioral toolbox now available for the zebrafish makes this species an attractive model for integrated analyses of chemical effects spanning behavior to molecular effect mechanisms.