Demasculinization and feminization of male gonads by atrazine: Consistent effects across vertebrate classes

Tyrone B. Hayes, Lloyd L. Anderson, Val R. Beasley, Shane R. de Solla, Taisen Iguchi, Holly Ingraham, Patrick Kestemont, Jasna Kniewald, Zlatko Kniewald, Valerie S. Langlois, Enrique H. Luque, Krista A. McCoy, Monica Munoz-de-Toro, Tomohiro Oka, Cleida A. Oliveira, Frances Orton, Sylvia Ruby, Miyuki Suzawa, Luz E. Tavera-Mendoza, Vance L. TrudeauAnna Bolivar Victor-Costa, Emily Willingham

Research output: Contribution to journalArticle

177 Citations (Scopus)

Abstract

Atrazine is the most commonly detected pesticide contaminant of ground water, surface water, and precipitation. Atrazine is also an endocrine disruptor that, among other effects, alters male reproductive tissues when animals are exposed during development. Here, we apply the nine so-called “Hill criteria” (Strength, Consistency, Specificity, Temporality, Biological Gradient, Plausibility, Coherence, Experiment, and Analogy) for establishing cause–effect relationships to examine the evidence for atrazine as an endocrine disruptor that demasculinizes and feminizes the gonads of male vertebrates. We present experimental evidence that the effects of atrazine on male development are consistent across all vertebrate classes examined and we present a state of the art summary of the mechanisms by which atrazine acts as an endocrine disruptor to produce these effects.

Atrazine demasculinizes male gonads producing testicular lesions associated with reduced germ cell numbers in teleost fish, amphibians, reptiles, and mammals, and induces partial and/or complete feminization in fish, amphibians, and reptiles. These effects are strong (statistically significant), consistent across vertebrate classes, and specific. Reductions in androgen levels and the induction of estrogen synthesis – demonstrated in fish, amphibians, reptiles, and mammals – represent plausible and coherent mechanisms that explain these effects. Biological gradients are observed in several of the cited studies, although threshold doses and patterns vary among species. Given that the effects on the male gonads described in all of these experimental studies occurred only after atrazine exposure, temporality is also met here. Thus the case for atrazine as an endocrine disruptor that demasculinizes and feminizes male vertebrates meets all nine of the “Hill criteria”.
Original languageEnglish
Pages (from-to)64-73
JournalJournal of Steroid Biochemistry and Molecular Biology
Volume127
Issue number1-2
DOIs
Publication statusPublished - Oct 2011
Externally publishedYes

Keywords

  • Atrazine
  • Gonads
  • Endocrine disruptor

Cite this

Hayes, T. B., Anderson, L. L., Beasley, V. R., de Solla, S. R., Iguchi, T., Ingraham, H., Kestemont, P., Kniewald, J., Kniewald, Z., Langlois, V. S., Luque, E. H., McCoy, K. A., Munoz-de-Toro, M., Oka, T., Oliveira, C. A., Orton, F., Ruby, S., Suzawa, M., Tavera-Mendoza, L. E., ... Willingham, E. (2011). Demasculinization and feminization of male gonads by atrazine: Consistent effects across vertebrate classes. Journal of Steroid Biochemistry and Molecular Biology, 127(1-2), 64-73. https://doi.org/10.1016/j.jsbmb.2011.03.015