Impact of prenatal stress on offspring glucocorticoid levels: A phylogenetic meta-analysis across 14 vertebrate species

Zaneta M. Thayer, Meredith A. Wilson, Andrew W. Kim, Adrian V. Jaeggi
2018 Scientific Reports  
Prenatal exposure to maternal stress is commonly associated with variation in Hypothalamic Pituitary Adrenal (HPA)-axis functioning in offspring. However, the strength or consistency of this response has never been empirically evaluated across vertebrate species. Here we meta-analyzed 114 results from 39 studies across 14 vertebrate species using Bayesian phylogenetic mixed-effects models. We found a positive overall effect of prenatal stress on offspring glucocorticoids (d' = 0.43) though the
more » ... 5% Highest Posterior Density Interval overlapped with 0 (−0.16-0.95). Meta-regressions of potential moderators highlighted that phylogeny and life history variables predicted relatively little variation in effect size. Experimental studies (d' = 0.64) produced stronger effects than observational ones (d' = −0.01), while prenatal stress affected glucocorticoid recovery following offspring stress exposure more strongly (d' = 0.75) than baseline levels (d' = 0.48) or glucocorticoid peak response (d' = 0.36). These findings are consistent with the argument that HPA-axis sensitivity to prenatal stress is evolutionarily ancient and occurs regardless of a species' overall life history strategy. These effects may therefore be especially important for mediating intra-specific life-history variation. In addition, these findings suggest that animal models of prenatal HPA-axis programming may be appropriate for studying similar effects in humans. Maternal effects are maternal influences on offspring phenotype that are independent of genotype 1 . Since the environment experienced during individual development may not be indicative of longer term trends, maternal effects allow organisms to developmentally adapt in response to a mother's life-long signal of environmental experience 2,3 . While these effects have been reported in a wide range of species, the question of whether the capacity for maternal effects quantitatively varies across species varying in phylogeny and life history characteristics is not well understood. Such findings are important since they inform our understanding of how evolutionarily ancient this response may be, as well as under what ecological conditions such effects may be adaptive 4 . In addition, given the proposed role of maternal effects in the developmental origins of adult health and disease (DOHaD) hypothesis 5 , an important question is whether the use of animal models is helpful for understanding these effects in humans. One of the most consistently studied exposures in the maternal effects literature is maternal stress. Maternal stress is an important signal of environmental conditions, and, when experienced prenatally, has been associated with morphological, behavioral, and physiological changes in a broad range of vertebrate offspring 6 . In a particularly impressive observational study that tracked the 10-year predator-prey cycle among snowshoe hares and lynxes, researchers found increased lynx density correlated with a reduction in birth size and more predator avoidant behaviors in hare offspring 7 . While maternal stress effects are sometimes interpreted as reflecting pathological impacts of prenatal stress exposure, such responses may also represent adaptive, fitness-enhancing adjustments for offspring and/or their mothers 4 . For example, being born into a high-predator environment could indicate elevated extrinsic mortality risk. Therefore maternal and offspring fitness may be enhanced by offspring
doi:10.1038/s41598-018-23169-w pmid:29563562 pmcid:PMC5862967 fatcat:5gsh3p6z2fco5poh5xjjwww7nu