Bisphenol A induces sex-dependent alterations in the dynamics of neuroendocrine seasonal adaptation in Djungarian hamsters

Abstract

AbstractIn nature, species synchronize reproduction and energy metabolism with seasons to optimize survival and growth. While the effects of endocrine-disrupting chemicals (EDCs) exposure on conventional laboratory rodents are increasingly studied, their impacts on mammalian seasonal adaptation remain unexplored. This study investigates the effect of oral exposure to bisphenol A (BPA) on physiological and neuroendocrine seasonal adaptation in Djungarian hamsters. Adult female and male hamsters were orally exposed to BPA (5, 50, or 500 µg/kg/d) or vehicle during a 10-week transition from a long (LP) to short (SP) photoperiod (winter transition) or vice versa (summer transition). Changes in body weight, food intake, and pelage color were monitored weekly and, at the end of the exposure, gene expression of hypothalamic markers of photoperiodic, reproductive and metabolic integration, reproductive organ activity, and glycemia were assessed. Our results revealed sex-specific effects of BPA on acquiring SP and LP phenotypes. During LP to SP transition, females exposed to 500 µg/kg/d BPA exhibited delayed body weight loss and reduced feed efficiency associated with a lower expression ofsomatostatinin the arcuate nucleus (ARC), while males exposed to 5 µg/kg/d BPA showed an accelerated acquisition of SP-induced metabolic parameters. During SP to LP transition, females exposed to 5 µg/kg/d BPA displayed a faster LP adaptation in reproductive and metabolic parameters, along with quicker ARC kisspeptin downregulation and delayed ARCPomcupregulation, while males exposed to BPA exhibited decreased expression of central photoperiodic integrators without changes in the physiological LP acquisition. This pioneering study investigating EDC impacts on mammalian seasonal physiology shows that BPA alters the dynamic of metabolic adaptation to both SP and LP transitions with marked sex dimorphism, causing temporal discordance in seasonal adaptation between males and females. These findings emphasize the importance of investigating EDCs’ impact on non-conventional animal models, providing insights into wildlife physiology.HighlightsDjungarian hamster’s seasonal adaptation is disrupted by BPA oral exposureBPA delays in females and accelerates in males the metabolic adaptation to short daysBPA accelerates in females, not in males, metabolic/reproductive adaptation to long daysBPA affects the photoperiodic expression of central reproductive and metabolic genesGraphical abstract