Stress-induced maternal effects on offspring: linking multivariate egg investment to environmental quality

Hormone-mediated maternal effects can shape offspring development in variable environmental conditions resulting in adaptive behavioral phenotypes. Numerous hormones can vary with environmental conditions and lead to different adaptive offspring responses. However, most of what we know about hormone-mediated maternal effects comes from studies on individual hormones even though the endocrine response to the environment is multifaceted and complex. Physiological stress responses in mothers may lead to greater offspring exposure to glucocorticoids or influence the allocation of other classes of maternal steroids (e.g. androgens, estrogens, progestogens) and any of these hormones may induce adaptive responses in offspring. Examining how the multivariate suite of yolk hormones responds to ecologically relevant environmental variation in natural systems is critical for assessing their role as potential cues of environmental conditions. Female western bluebirds (Sialia mexicana) in challenging environmental conditions have increased circulating glucocorticoids and produce better adapted offspring that are more aggressive and are more likely to disperse. We used this well-characterized adaptive maternal effect to test the functional importance of multiple classes of steroids using liquid chromatography-mass spectrometry (LC-MS-MS). We found that in more challenging environments - fewer nest sites, smaller territories - the multivariate yolk steroid profile shifted, with the strongest change in glucocorticoid metabolites, suggesting that maternal glucocorticoid processing varies with ecological context. We also found that estrone and etiocholanolone, but not other androgens, covaried with maternal environment. Overall, our results advance our understanding of the mechanisms underlying adaptive maternal effects in nature and highlight novel steroid pathways that may influence offspring phenotypes.