Stress hormone masculinizes female morphology and behaviour

Abstract

Sex steroids play major roles in vertebrate sexual differentiation. Unexpectedly, we now find that exposure to elevated levels of the naturally occurring stress hormone cortisol can also masculinize sexually dimorphic morphological characters and behaviour in adult female mosquitofish (Gambusia affinis) in a dose-dependent manner. Females masculinized by cortisol developed elongated anal fins with distal tip features similar to those of mature males. Most masculinized females also attempted to copulate when placed with normal females. Although the mechanism of masculinization is currently unknown, we propose a role for an enzyme that both inactivates cortisol and catalyzes the final step in synthesis of a major teleost androgen. This mechanism may also help explain some previously reported effects of stress on sexual development across vertebrate taxa. Our findings underscore the need to understand the full range of chemicals, both naturally occurring hormones and human-produced endocrine disruptors, that can influence sexual differentiation and reproductive function.

Figure 1.

Cortisol-induced masculinization of adult female mosquitofish. Anal fins of (a) normal female, (b) cortisol-exposed female and (c) normal male. (d) Anal fin of a cortisol-treated female illustrating ray length measurements (black lines) used to calculate the masculinization index (see text). (e) Distal tip structures on the anal fin of a cortisol-treated female (alizarin stain). Scale bars, (a–c) 1 mm.

Figure 2.

Variation in masculinization of adult female mosquitofish with cortisol concentration. (a) Masculinization index among cortisol treatments and controls over two experiments (n = 5–25). Grey bars, experiment 1; white bars, experiment 2. (b) Copulation attempts by control and cortisol-treated females (n = 5–12) and normal males (n = 8). Male copulation attempts are towards control females exposed to water only.