Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A

Abstract

Exposure to endocrine disrupting compounds (EDCs), such as bisphenol A (BPA), may cause adverse health effects in wildlife and humans, but controversy remains as to what traits are most sensitive to EDCs and might serve as barometers of exposure. Expression of sexually selected traits that have evolved through intrasexual competition for mates and intersexual choice of mating partner are more dependent on developmental and physical condition of an animal than naturally selected traits and thus might be particularly vulnerable to disruption by developmental exposure to EDCs. We have used the deer mouse (Peromyscus maniculatus) as a model to test this hypothesis. Adult male-male competition for mates in this species is supported by enhanced spatial navigational and exploratory abilities, which enable males to search for prospective, widely dispersed females. Male deer mice exposed to BPA or ethinyl estradiol (EE) through maternal diet showed no changes in external phenotype, sensory development, or adult circulating concentrations of testosterone and corticosterone, but spatial learning abilities and exploratory behaviors were severely compromised compared with control males. Because these traits are not sexually selected in females, BPA exposure predictably had no effect, although EE-exposed females demonstrated enhanced spatial navigational abilities. Both BPA-exposed and control females preferred control males to BPA-exposed males. Our demonstration that developmental exposure to BPA compromises cognitive abilities and behaviors essential for males to reproduce successfully has broad implications for other species, including our own. Thus, sexually selected traits might provide useful biomarkers to assess risk of environmental contamination in animal and human populations.mate choice | sexual selection | spatial abilities | cognition | sex differences D evelopmental exposure to endocrine-disrupting compounds (EDCs) has posed a major threat to wildlife since the largescale production of these industrial chemicals (1). Numerous studies have documented disturbances of sex-typical development, reproductive tract pathologies, and abnormal adult behaviors through environmental contact with EDCs, including bisphenol A (BPA) (2-7). However, scant information is available regarding exposure to EDCs during development within the context of sexual selection (8, 9). Expression of sexually selected traits is critical to reproductive fitness and may be particularly vulnerable to EDCs because these traits show greater phenotypic variation than naturally selected traits, owing in part to dependence on more genetic loci and overall body condition (10, 11). Moreover, optimal expression of these traits in adulthood requires a complex orchestration of developmental exposure to estrogens and androgens, processes that can be compromised by EDC exposure (3, 4). We predicted that traits that evolved through intrasexual competition for mates and influence intersexual choice of mating partner would be particularly sensitive to EDCs (3, ...

Maternal bisphenol A (BPA) decreases attractiveness of male offspring

“…One of the prominent effects of early BPA exposure is that it eliminates a number of sex differences in brain and behavior, as seen in the Jašarevic′ study (1). Elimination of these sex differences may not only disrupt reproductive behaviors but could change the physiology of females and males.…”

“…In the study by Jašarevic′ et al (1), maternal behavior was not examined in the deer mice. However, maternal BPA exposure does influence rodent maternal behavior, as exposed dams spend less time licking their pups and on the nest.…”

“…The expression of sexually dimorphic spatial ability depends on both early (pre-or perinatal) and adult levels of sex hormones in rodents (3). The report by Jašarevic′ et al (1) shows that these sexually dimorphic traits, spatial ability and exploratory behavior, in addition to attractiveness, are affected by maternal dietary exposure to the environmental endocrine disrupter BPA. Specifically, the authors show that maternal consumption of low levels of dietary BPA renders male offspring at a disadvantage for mating, not only because of poorer spatial navigation and greater anxiety-like behavior but also because they are less attractive to female conspecifics.…”

“…Your clothes? Findings from a new study (1) suggest it may be your mother's dietary exposure to bisphenol A (BPA). In the study published in PNAS, Jašarevic′ et al (1) find that maternal BPA exposure impairs spatial ability, decreases exploratory behavior, and reduces attractiveness of male deer mice progeny.…”

“…Findings from a new study (1) suggest it may be your mother's dietary exposure to bisphenol A (BPA). In the study published in PNAS, Jašarevic′ et al (1) find that maternal BPA exposure impairs spatial ability, decreases exploratory behavior, and reduces attractiveness of male deer mice progeny. These traits are sexually dimorphic and are subjected to sexual selection because they are essential characteristics needed to find mates and reproduce in male deer mice (and other polygynous species) (2).…”