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

MacLeod, Kirsty J. LU ; While, Geoffrey M. LU and Uller, Tobias LU (2021) In Ecology and Evolution 11(23). p.17238-17259
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... (More)

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.

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author
; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
glucocorticoids, maternal effects, maternal stress, meta-analysis, viviparity
in
Ecology and Evolution
volume
11
issue
23
pages
22 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:85120358061
  • pmid:34938505
ISSN
2045-7758
DOI
10.1002/ece3.8360
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
id
758c6f56-7782-4315-92f1-681e9d44caa9
date added to LUP
2022-01-24 09:13:50
date last changed
2024-06-16 00:19:09
@article{758c6f56-7782-4315-92f1-681e9d44caa9,
  abstract     = {{<p>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.</p>}},
  author       = {{MacLeod, Kirsty J. and While, Geoffrey M. and Uller, Tobias}},
  issn         = {{2045-7758}},
  keywords     = {{glucocorticoids; maternal effects; maternal stress; meta-analysis; viviparity}},
  language     = {{eng}},
  month        = {{12}},
  number       = {{23}},
  pages        = {{17238--17259}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Ecology and Evolution}},
  title        = {{Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers}},
  url          = {{http://dx.doi.org/10.1002/ece3.8360}},
  doi          = {{10.1002/ece3.8360}},
  volume       = {{11}},
  year         = {{2021}},
}