Mate choice, sexual selection, and endocrine-disrupting chemicals

Abstract

Humans have disproportionately affected the habitat and survival of species through environmental contamination. Important among these anthropogenic influences is the proliferation of organic chemicals, some of which perturb hormone systems, the latter referred to as endocrine-disrupting chemicals (EDCs). EDCs are widespread in the environment and affect all levels of reproduction, including development of reproductive organs, hormone release and regulation through the life cycle, the development of secondary sexual characteristics, and the maturation and maintenance of adult physiology and behavior. However, what is not well-known is how the confluence of EDC actions on the manifestation of morphological and behavioral sexual traits influences mate choice, a process that requires the reciprocal evaluation of and/or acceptance of a sexual partner. Moreover, the outcomes of EDC-induced perturbations are likely to influence sexual selection; yet this has rarely been directly tested. Here, we provide background on the development and manifestation of sexual traits, reproductive competence, and the neurobiology of sexual behavior, and evidence for their perturbation by EDCs. Selection acts on individuals, with the consequences manifest in populations, and we discuss the implications for EDC contamination of these processes, and the future of species.

Keywords: Complementarity; Endocrine-disrupting chemicals; Evolution; Mate choice; Mate compatibility; Reproduction; Sexual selection.

Figure 1

Model of the complementarity of the sexes during mating. The male and female must interact, assess and choose a mate. In nature this is a mutual choice and is dependent upon a variety of conditions. Changes in the environment, such as EDCs, act upon individuals throughout their life history. If exposure occurs early in life, the entire sexual phenotype can change, rendering such individuals as adults infertile or unable to communicate and perceive signals from other individuals properly. The interaction is reciprocal, which includes both the hormonal feedback loop within each individual (hypothalamic-pituitary-gonadal axis) as well as between the individual and its immediate environment. Within the brain two nuclei, the medial preoptic area (mPOA) and the ventromedial nucleus (VMN) also play complementary roles, where activity in one typically diminishes activity in the latter. The unit of selection in this context is the mating pair, and its reproductive success is paramount for life and evolution. Modified from Crews, 1977.