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

Interdisciplinary Neuroscience Program, Bond Life Sciences Center, and Department of Biological Sciences, University of Missouri, Columbia, MO 65211, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 06/2011; 108(28):11715-20. DOI: 10.1073/pnas.1107958108
Source: PubMed

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.

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    • "Their ubiquitous presence in North America also means that Peromyscus is found at many sites contaminated with toxic chemicals and may be useful as biomarkers of contamination . Peromyscus has been employed in numerous studies on the responses to chemicals, such as PCBs (Voltura and French 2007) and Aroclor 1254 (Wu et al. 1999) as well as being used to demonstrate transgenerational effects of BPA exposure (Jasarevic et al. 2011). "
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    ABSTRACT: The rodent genus Peromyscus is the most numerous and species-rich mammalian group in North America. The naturally occurring diversity within this genus allows opportunities to investigate the genetic basis of adaptation, monogamy, behavioral and physiological phenotypes, growth control, genomic imprinting, and disease processes. Increased genomic resources including a high quality genetic map are needed to capitalize on these opportunities. We produced interspecific hybrids between the prairie deer mouse (P. maniculatus bairdii) and the oldfield mouse (P. polionotus) and scored meiotic recombination events in backcross progeny. A genetic map was constructed by genotyping of backcross progeny at 185 gene-based and 155 microsatellite markers representing all autosomes and the X-chromosome. Comparison of the constructed genetic map with the molecular maps of Mus and Rattus and consideration of previous results from interspecific reciprocal whole chromosome painting allowed most linkage groups to be unambiguously assigned to specific Peromyscus chromosomes. Based on genomic comparisons, this Peromyscus genetic map covers ~83 % of the Rattus genome and 79 % of the Mus genome. This map supports previous results that the Peromyscus genome is more similar to Rattus than Mus. For example, coverage of the 20 Rattus autosomes and the X-chromosome is accomplished with only 28 segments of the Peromyscus map, but coverage of the 19 Mus autosomes and the X-chromosome requires 40 chromosomal segments of the Peromyscus map. Furthermore, a single Peromyscus linkage group corresponds to about 91 % of the rat and only 76 % of the mouse X-chromosomes.
    Mammalian Genome 01/2014; 25(3-4). DOI:10.1007/s00335-014-9500-8 · 2.88 Impact Factor
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    • "Thirty mg/kg CDPPB prior to daily reversal training trials enhanced reversal learning performance in the Barnes maze, as demonstrated by decreased latencies to locate the escape hole and fewer errors committed during the second day of reversal training. Additionally, CDPPB administration increased the proportion of animals utilizing a spatial search, which is a more efficient search strategy generally associated with increased performance levels (Harrison et al., 2006; Jasarevic et al., 2011). Animals treated with 30 mg/kg CDPPB also displayed enhanced performance when the contingency was shifted as "
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    ABSTRACT: Metabotropic glutamate receptor 5 (mGlu5) has been implicated in a variety of learning and memory processes and is important for avoidance learning. The present studies used an mGlu5 receptor positive allosteric modulator, 3-cyano-N-(1,3 diphenyl-1H-hyrazol-5-yl)benzamide (CDPPB), to characterize the importance of mGlu5 receptors in aversively- and appetitively-motivated spatial learning tasks (tasks in which the instrumental contingency involves discriminative cues that differ in spatial location). C57Bl/6 male mice were initially trained in the Barnes maze in the absence of drug. Subsequently, CDPPB (30 mg/kg, i.p.), administered 20 min prior to each of 3 daily reversal learning training sessions in the Barnes maze, significantly enhanced performance compared to vehicle-treated controls and had a significant effect on search strategy. Mice treated with CDPPB also displayed significantly less perseverative behavior than control-treated animals. In a second experiment, male Sprague-Dawley rats were trained in an appetitively-motivated, delayed alternation version of a T-maze. 30 mg/kg CDPPB (s.c.), delivered 20 min prior to each of 5 daily training sessions, enhanced the delay rats were able to withstand between the sample and choice portions of each T-maze trial. The present results emphasize the role of mGlu5 receptors in spatial learning tasks and support previous studies which report mGlu5 positive allosteric modulators can enhance learning in some tasks and may have potential as nootropic drugs.
    Neurobiology of Learning and Memory 11/2012; 99. DOI:10.1016/j.nlm.2012.10.010 · 4.04 Impact Factor
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    • "One week after the animals were tested in the Barnes maze, their exploratory and anxiety-like behaviours were measured by using the elevated plus maze (EPM), as described previously (Fountain et al. 2008; Ja sarevi c et al. 2011). The EPM was constructed of black polypropylene in a plus configuration with two opposite open arms (30 cm), a middle platform (5 Â 5 cm) and two opposing closed arms (30 cm). "
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    ABSTRACT: A male advantage in spatial abilities is predicted to evolve in species where males rely on expansion of home territory to locate dispersed mates during the breeding season. We sought to examine mechanistic underpinnings of this evolved trait by comparing spatial navigational abilities in two species of Peromyscus that employ widely different reproductive strategies. Males and females from outbred stocks of deer mice (P. maniculatus bairdii) in which males engage in territorial expansion and mate search and California mice (P. californicus insignis), in which males do not, were administered tasks that assessed spatial learning and memory, and activity and exploratory behaviours. The maze employed for these studies included four spatial cues that could be used to aid in locating 1 of 12 potential escape holes. As predicted, male deer mice outperformed conspecific females and California mice males in maze performance and memory, and this difference appeared to be due to extent to which animals used spatial cues to guide maze navigation. Consistent with territorial expansion as a component of competition for mates, male deer mice were more active and engaged in more exploratory and less anxiety-related behaviours than conspecific females and California mice males. The results have implications for understanding and studying the cognitive and behavioural mechanisms that have evolved through male-male competition that involves territorial expansion and mate search.
    Animal Behaviour 11/2012; 84(5):1141-1149. DOI:10.1016/j.anbehav.2012.08.015 · 3.07 Impact Factor
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