Maternal Effects in Mammals is an authoritative volume that provides a comprehensive
review of new developments on a topic of importance in evolutionary biology, developmental
psychology, and biomedical research. Maternal effects are defined here as effects
of the mother’s phenotype on offspring phenotype, separate from the direct effects
of genes inherited from the mother. It has been a decade since the publication of
Maternal Effects as Adaptations (Mousseau and Fox 1998) brought this topic to the
forefront in population biology. This edited volume builds on that earlier work, with
a focus on mammals. The features that define the mammalian order, internal gestation,
lactation and maternal care, make mammalian mothers particularly good candidates for
exhibiting maternal effects on the health and fitness of their offspring. For many
mammalian species, these early influences are augmented by an extended period of immaturity
and continuing relationships between mothers and offspring into adulthood. As the
chapters in this volume demonstrate, maternal effects can be a powerful force influencing
individual development and the evolution of populations.
The book is composed of 14 chapters that cover the theoretical basis in population
biology, review the wealth of new data demonstrating maternal effects in different
mammalian groups, and provide evidence for some of the proximate mechanisms that mediate
maternal effects on offspring phenotypes. It is noteworthy that a large percentage
of the material referenced here has appeared in the last decade, and includes the
use of a number of new molecular genetics technologies. This volume also expands the
topic of maternal effects into new physiological, social, and behavioral domains.
After a brief introduction by the editors, the book begins with two chapters that
present the theoretical background for maternal effects using quantitative evolutionary
biological models. Cheverud and Wolf illustrate the complexity of maternal effects
in a model that includes components for genetic and environmental influences on the
mother’s phenotypes, direct genetic and environmental effects on offspring phenotypes,
and a possibility of interactions of maternal effects with offspring genotype and
with current environment. The resulting model predicts that maternal effects can accelerate,
slow, and even reverse the direction of selection on offspring traits alone, depending
on the direction and degree of genetic covariance between maternal and offspring effects.
In Chapter 3, Wade, Priest, and Cruikshank present a fitness model of maternal effects
that reflects the theory of Relaxed Selective Constraint. They then take an innovative
approach to testing the theory using molecular genetic sequence data and gene expression
profiles for a maternal effects gene in mice. An interesting feature of these analyses
is that much of the data came from publicly available shared resources in GenBank.
These two theoretical chapters provide information on quantitative approaches to evolutionary
biology modeling, combined with the use of experimental methods and new genetic technologies
to test predictions from the models. They also underscore the pitfalls of ignoring
maternal effects if the goal is to understand population level evolutionary processes.
This point is supported empirically in the chapter by McAdam that effectively documents
the impact of maternal effects on population cycles in red squirrels.
Most of the chapters that follow focus on demonstrating maternal effects in specific
taxonomic groups. For example, Wilson and Festa-Bianchet (Chapter 5) and Bowen (Chapter
6) review the extensive body of information available on maternal effects in wild
ungulates and pinnipeds. Because both ungulates and pinnipeds are relatively easy
to follow and observe in the wild, studies have been able to provide consistent evidence
for effects of mother’s age, experience, and condition on offspring survival, birth
weight, and early growth rate in different species. This research also suggests that
both environmental and genetic maternal effects are involved in influencing offspring
development, and that genetic maternal effects may be more evident under some environmental
circumstances than others.
Several chapters in this volume take a more behavioral and physiological approach
to maternal effects, with consideration of proximate mechanisms that mediate between
maternal phenotypes and offspring outcomes. For example, Maestripieri expands the
scope of maternal effects beyond growth and physical development in his chapter on
maternal effects in primates. Research in captive and provisioned free-ranging populations
has provided evidence of maternal effects on offspring social behavior, social preferences,
reactivity to the environment, and intergenerational transmission of maternal behavior.
Galef presents an interesting chapter on the many ways mammalian mothers influence
the food choices and feeding behavior of their offspring. Mateo reviews studies of
the effects of prenatal exposure to maternal hormones and the effects of postnatal
physical environment and maternal care on offspring development across taxonomic groups.
In an example from her own research, she describes the role of the mother in the behavioral
and glucocorticoid response to predators in Belding’s ground squirrels. Holekamp and
Dloniak cover hormonal and behavioral effects in a review of maternal effects in fissiped
carnivores, including data on the relationship between mother’s dominance rank and
androgen levels during pregnancy and the later sexual and aggressive behavior of juvenile
offspring in wild spotted hyenas. An interesting twist on maternal gestational effects
is provided by Vandenbergh in a chapter that describes the persistent effects of intrauterine
position on development in rodents. Female fetuses located between two male fetuses
are exposed to levels of androgens that can influence brain development and have lifelong
effects on morphology, behavior, and reproduction. Unlike most other maternal effects
described in this volume, however, intrauterine position may be better considered
an effect of sibling phenotypes on individual development than of maternal phenotypes.
A noteworthy chapter by Champagne and Curley (Chapter 9) provides information on an
epigenetic mechanism that can mediate maternal effects. Methylation of specific sites
in promoter regions of genes is known to prevent RNA access and keep the methylated
genes in an inactive state. Because DNA methylation patterns are maintained through
cell division, they can result in persistent reductions in expression of the gene
in that tissue. This process has now been shown to mediate effects of natural variation
in maternal care on offspring behavior and stress reactivity in rats. Offspring that
experienced a lower quality of maternal care had higher levels of DNA methylation
and reduced gene expression in hippocampal glucocorticoid receptors. The importance
of DNA methylation in this process was verified when treatment of the offspring with
agents that promote demethylation reversed the differences produced by the lower quality
care. This type of controlled experimental research provides a necessary supplement
to the more naturalistic and uncontrolled results presented in other chapters.
The book ends with a discursive chapter by Bjorklund, Grotuss, and Csinady on the
possible role of maternal effects in the evolution of human intelligence, followed
by a summary of the book by the editors. Mateo and Maestripieri call for more interdisciplinary
research with greater attention to research on proximate mechanisms that mediate maternal
effects on offspring outcomes. They also suggest more longitudinal studies of wild
populations using within female designs and consideration of possible sex differences
in maternal effects on offspring development.
Together, these chapters support the importance of maternal effects on individual
development and on evolutionary processes. Effects on offspring phenotypes are particularly
strong during early development and tend to decline with offspring age and independence
from the mother. For some outcomes, however, maternal effects can be measured in the
next generation. At the level of the population, maternal effects can exceed direct
genetic effects in explaining trait variance, and can exert strong effects on the
pace and direction of selection.
One notable omission in this volume is a chapter on fetal programming theory. The
theory and supporting data that maternal nutrition during gestation has lifelong consequences
for offspring health through early programming of metabolic processes are only briefly
mentioned here. Further consideration of this literature would have made the volume
of greater interest to biomedical scientists studying metabolic disorders like obesity,
hypertension, diabetes, and cardiovascular disease. Another weakness in many of the
chapters is the tendency to label correlations between maternal and offspring phenotypes
as maternal effects without acknowledging the need to control for direct genetic or
environmental effects on offspring traits.
Who should read this book? Most of the chapters are written at an advanced level and
assume some prior knowledge of terminology and theory. As a result, this volume would
be most appropriate for upper division students, graduate students, post docs, and
practitioners in the field. This is a particularly important book to read for biomedical
geneticists who are not, as yet, considering maternal effects in the search for genetic
influences on human diseases and disorders. It would also be of value for developmental
and biobehavioral psychologists interested in parental influences on offspring development.
This book achieves the goal of synthesizing a large body of information, much of it
produced since the last volume on this topic was published. It is likely to promote
greater cross-disciplinary awareness, and stimulate further research in the field.