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. 2021 Nov 29;11(23):17238-17259.
doi: 10.1002/ece3.8360. eCollection 2021 Dec.

Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers

Kirsty J MacLeod  1 , Geoffrey M While  2 , Tobias Uller  1
Affiliations

Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers

Kirsty J MacLeod et al. Ecol Evol. .

Abstract

Maternal stress during gestation has the potential to affect offspring development via changes in maternal physiology, such as increases in circulating levels of glucocorticoid hormones that are typical after exposure to a stressor. While the effects of elevated maternal glucocorticoids on offspring phenotype (i.e., "glucocorticoid-mediated maternal effects") have been relatively well established in laboratory studies, it remains poorly understood how strong and consistent such effects are in natural populations. Using a meta-analysis of studies of wild mammals, birds, and reptiles, we investigate the evidence for effects of elevated maternal glucocorticoids on offspring phenotype and investigate key moderators that might influence the strength and direction of these effects. In particular, we investigate the potential importance of reproductive mode (viviparity vs. oviparity). We show that glucocorticoid-mediated maternal effects are stronger, and likely more deleterious, in mammals and viviparous squamate reptiles compared with birds, turtles, and oviparous squamates. No other moderators (timing and type of manipulation, age at offspring measurement, or type of trait measured) were significant predictors of the strength or direction of the phenotypic effects on offspring. These results provide evidence that the evolution of a prolonged physiological association between embryo and mother sets the stage for maladaptive, or adaptive, prenatal stress effects in vertebrates driven by glucocorticoid elevation.

Keywords: glucocorticoids; maternal effects; maternal stress; meta‐analysis; viviparity.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Orchard plot showing overall glucocorticoid‐mediated maternal effects on offspring traits. Position on the x‐axis corresponds to effect size value (Hedges’ g), with spread on the y‐axis based on quasi‐random noise; point size reflects precision, and k indicates number of effect sizes (Nakagawa et al., 2021). A dashed vertical line marks 0, that is, no effects, to allow interpretation of direction of effects. Meta‐analytical mean (estimate and error) is shown as a filled, outlined point, and confidence intervals as a black bar
FIGURE 2
FIGURE 2
Forest plots showing that there were significantly more negative outcomes of glucocorticoid‐mediated maternal effects in viviparous relative to oviparous species in (ai) the full dataset and (bi) in squamate reptiles. The magnitude (|g|, i.e., absolute effects) of prenatal stress was also stronger in (aii) viviparous species overall, though this effect was not apparent in the squamates (bii)
See this image and copyright information in PMC

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