Disruption of Parenting Behaviors in California Mice, a Monogamous Rodent Species, by Endocrine Disrupting Chemicals

Abstract

The nature and extent of care received by an infant can affect social, emotional and cognitive development, features that endure into adulthood. Here we employed the monogamous, California mouse (Peromyscus californicus), a species, like the human, where both parents invest in offspring care, to determine whether early exposure to endocrine disrupting chemicals (EDC: bisphenol A, BPA; ethinyl estradiol, EE) of one or both parents altered their behaviors towards their pups. Females exposed to either compound spent less time nursing, grooming and being associated with their pups than controls, although there was little consequence on their weight gain. Care of pups by males was less affected by exposure to BPA and EE, but control, non-exposed females appeared able to “sense” a male partner previously exposed to either compound and, as a consequence, reduced their own parental investment in offspring from such pairings. The data emphasize the potential vulnerability of pups born to parents that had been exposed during their own early development to EDC, and that effects on the male, although subtle, also have consequences on overall parental care due to lack of full acceptance of the male by the female partner.

Effects of developmental exposure to bisphenol A on spatial navigational learning and memory in rats: A CLARITY-BPA study

“…This has been shown to occur in various rodent models where the dams are exposed to BPA and/or related EDC (Boudalia et al, 2014; Cummings et al, 2005; Della Seta et al, 2005; Engell et al, 2006; Johnson et al, 2015; Kundakovic et al, 2013; Palanza et al, 2002). Potential poor parenting received by the BPA-exposed pups may place them at risk for learning and memory deficiencies and other behavioral deficits (Birnie et al, 2013; Dougherty et al, 2013; Parent et al, 2013).…”

Neuroendocrine disruption in animal models due to exposure to bisphenol A analogues

“…For instance, mice and deer mice ( Peromyscus maniculatus bairdii ) developmentally exposed to environmentally relevant concentrations of BPA show increased anxiety-like behaviors [17; 71; 72; 73; 74; 75]. Several rodent studies have shown that BPA exposure can reduce maternal and even paternal care [15; 22; 72; 76]. The current studies indicate that BPA-alternatives can alter gene involved in the dopamine-serotonin systems in the prefrontal cortex, which might account for some of the observed behavioral disruptions [65].…”

“…However, it is also becoming apparent that exposure to BPA, especially during development, can result in neurobehavioral and other disorders [2; 3; 4; 5; 6; 7; 8; 9; 10; 11; 12; 13; 14]. Examples of neurobehavioral disorders that have been associated with BPA in rodent and other animal models include cognitive deficits, increased anxiety, socio-sexual deficiencies, compromised maternal and/or paternal care, and decreased voluntary physical activity [15; 16; 17; 18; 19; 20; 21; 22; 23]. Evidence also links exposure to this chemical to neurological disorders, such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD) [2; 3; 4; 5; 6; 7; 8; 9; 10; 11; 24; 25; 26; 27].…”

Perinatal exposure to endocrine disruptors: sex, timing and behavioral endpoints

“…In the California mouse, a monogamous species with bi-parental care, prenatal and neonatal exposure of mice to BPA decreased subsequent maternal behavior in females. Although paternal behavior was not significantly affected by BPA exposure, females paired with BPA-exposed males showed reduced engagement in maternal care [34•]. Accordingly, male deer mice that were perinatally exposed to BPA were less attractive for females, which preferred unexposed control males to BPA-exposed males in a mate choice test [14].…”

“…Maternal exposure during pregnancy through a non-stressful administration procedure (i.e., allowing pregnant female mice to drink corn oil in which the compound is dissolved) to a low, environmentally relevant dose of BPA produced subtle alterations in subsequent maternal behavior and in their offspring’s behavioral development [5]. Further studies in rats [33,54], mice [12••], voles [55] and Peromyscus (P. California; [34•]) have confirmed that maternal behavior can be altered by exposure to BPA and other EDCs during gestation and lactation. It is well known that variation in maternal care can be responsible for differences in offspring in the rate of maturation, such as growth rate, and the subsequent neuroendocrine and behavioral responses associated with epigenetic changes [56].…”