Long-term effects of in ovo exposure to an environmentally relevant dose of atrazine on the thyroid gland of Caiman latirostris

Abstract

The increased incidence of human thyroid disorders, particularly in women, suggests that the exposure to endocrine-disrupting compounds (EDCs) together with sex-related factors could play a role in thyroid dysregulation. Since the herbicide atrazine (ATZ) is an environmental EDC suspected to behave as a thyroid disruptor, and Caiman latirostris is a crocodilian species highly sensitive to endocrine disruption that can be exposed to ATZ, this study aimed to describe the histoarchitecture and sexually dimorphic features of the thyroid gland of C. latirostris, and to determine the long-term effects of in ovo exposure to an environmentally relevant dose of ATZ (0.2 ppm) on its thyroid gland and growth. Control caimans showed no sexual dimorphisms. In contrast, ATZ-exposed caimans showed altered embryo growth but an unaltered temporal pattern of development and a sexually dimorphic response in the body condition index growth curves postnatally, which suggests a female-related increase in fat storage. Besides, both male and female exposed caimans showed increases in the size of the thyroid stromal compartment, content of interstitial collagen, and follicular hyperplasia, and decreases in the expression of androgen receptor in the follicular epithelium. ATZ-exposed females, but not males, also showed evidences of thyroid enlargement, colloid depletion, increased follicular epithelial height and increased presence of microfollicular structures. Our results demonstrate that prenatal exposure of caimans to ATZ causes thyroid disruption and that females were more vulnerable to ATZ than males. The effects were organizational and observed long after exposure ended. These findings alert on ATZ side-effects on the growth, metabolism, reproduction and development of non-target exposed organisms, particularly females.