Download Maternal Effects in Animal Ecology1

AMER. ZOOL., 36:83-105 (1996)
Maternal Effects in Animal Ecology1
JOSEPH BERNARDO
Department of Zoology, University of Texas, Austin, Texas 787J2
Maternal effects comprise a class of phenotypic effects that
parents have on phenotypes of their offspring that are unrelated to the
offspring's own genotype. Although biologists have known about the importance of these effects for decades, maternal effects have only recently
been studied widely by evolutionary ecologists. Moreover, the impact of
maternal effects on the rate and direction of evolution of other components of the phenotype has only recently been fully elucidated by theoretical genetic models. This paper provides a brief overview of maternal
effects research, focusing on research conducted in animal systems. First,
I review and summarize definitions and theoretical treatments of maternal
effects. Then I survey the diversity of maternal effects and some of the
kinds of ecological and evolutionary impacts that maternal effects have
been shown to have on offspring performance. Third, I discuss some of
the ecological and evolutionary implications of maternal effects in ecological research. In this context, it is argued that the kinds of maternal
effects that have been studied, and some of the potential implications of
maternal effects that have not been explored are both artifacts of research
effort. Hence, I identify several fruitful areas for future maternal effects
research. Lastly, I describe the necessity of explicitly incorporating maternal effects in ecological research, whether or not the researcher is focusing on them as the topic of the research.
SYNOPSIS.
ecological and evolutionary explanations of
Phenotypes have long been viewed as a phenotypic patterns and dynamics.
Maternal effects contribute complexity to
complex product of interaction between gephenotypes
of many traits, as well as to binotype and environment. As evolutionary
ologists'
attempts
to analyze phenotypes.
biology has aged, both empirical and theothe
latter
issue
has been long underWhile
retical insights have shown that even early
the pervasiveness
stood,
only
recently
have
perceptions of phenotypic complexity were
and
evolutionary
signifiand
ecological
incomplete. For example, quantitative geof
maternal
effects
become
widely
cance
netic models reveal that complex genetic
As
a
result,
explicit
incorpoappreciated.
correlation structure underlies most traits
that interest the ecologist or evolutionist ration of maternal effects into the study of
(review: Arnold, 1992), meaning that re- adaptive evolution is increasing rapidly.
sponses to selection in such traits may not Moreover, recent theoretical work has exalways be as rapid or predictable as for plored implications of the idea that matertraits that have a simpler genetic basis. nal effects may have a genetic component
These important insights have been inte- and so can evolve (Riska et al, 1985; Kirkgrated by many biologists into subsequent patrick and Lande, 1989; Cowley and Atchley, 1992; review in Arnold, 1994a). These
models reveal greater complexity in understanding phenotypic evolution when traits
1
From the Symposium Maternal Effects on Early are subject to maternal effects than might
Life History, Their Persistence, and Impact on Organ- have been imagined. Maternal effects can
ismal Ecology presented at the Annual Meeting of the
American Society of Zoologists, 27—30 December slow or accelerate the rate of evolution of
a character compared to the case when no
1993, at Los Angeles, California.
INTRODUCTION
83
84
JOSEPH BERNARDO
maternal effect is involved; maternal effects
can affect evolution of other characters,
sometimes even causing evolution in a direction opposite that favored by selection;
and maternal effects may allow evolution to
occur even after selection has ceased.
The implications of these findings extend
well beyond the theoretician's desk, and
they are profound, perhaps no more so than
for ecologists. The unusual dynamics of
traits subject to maternal effects suggest
that attempts to analyze or interpret variation in such traits will be incomplete, if not
misleading, when impacts of maternal effects are ignored. Indeed, progress in science is made when new findings are integrated into subsequent research. An important goal of this paper is to show how recent
findings from evolutionary theory about
maternal effects are relevant to ecological
analyses of phenotypic variation, particularly because maternal effects are prevalent
in the traits that ecologists often study.
The symposium upon which this paper is
based had three chief goals. The first was
to bridge various conceptual gaps in maternal effects research with a goal of identifying common threads in the ecological and
evolutionary significance of maternal effects, especially as they relate to the performance of immature stages early in ontogeny. One obvious gap has already been
suggested: that between evolutionary theory of maternal effects and ecological analysis of traits subject to maternal effects.
Much work on genetic aspects of maternal
effects and their impact upon evolutionary
dynamics of other traits has developed outside the conceptual life history framework
concerned with interpreting patterns of variation in propagule size, parental care, and
so on that have interested ecologists. Similarly, ecologists have made little effort to
integrate insights from evolutionary analyses of maternal effects into extensive study
of ecological consequences of maternal effects such as egg size. For example, ecologists might ask how egg size contributes
to variation in growth rate of immature
stages, and possibly, how these effects in
early ontogeny affect size or performance
at subsequent life cycle stages. A parallel
question, however, is to ask how variance
in egg size arises in the first place and
whether selection on propagule size entails
evolutionary and ecological responses for
other aspects of the phenotype in other parts
of the life cycle, (e.g., maternal size: Bernardo, 1994a). While it may be convenient
to think about and analyze complex phenotypes such as body size from a single
ecological perspective (e.g., body size
evolves as it does due to resource availability patterns, or due to competition with
a particular other species), such approaches
take little account of the diverse avenues of
selection to which body size must respond,
of which maternal effects may constitute an
important component.
Less obvious but large gaps exist within
the realm of ecological studies of maternal
effects. Ecologists have been studying certain maternal effects for many years; there
is a rich literature, for example, about the
impacts of egg, seed, or neonate size (hereafter "propagule size") on ecological phenomena ranging from survival and growth
to competition and predation. Nevertheless,
even this extensive body of work has proceeded in many taxa from different perspectives with limited exchange of ideas
(review: Bernardo, 1996). For instance, marine invertebrate workers have studied effects of egg size on both dispersal and
fertilization success (review: Levitan, 1993)
or developmental pattern (Strathmann,
1977, 1985, 1990, 1993; McEdward and
Janies, 1993; McEdward, 1996; and others),
but effects of egg size on offspring performance in the plankton (e.g., growth, survival, motility), a logistically challenging
problem, are scarcely explored. In contrast,
egg size effects on gametic dispersal and
fertilization are irrelevant or less obvious
problems for terrestrial vertebrates with internal fertilization. Rather, these workers focus on effects of egg size on early offspring
performance (Bernardo, 1991, 1996), possibly because it is easy to study this link
directly in terrestrial juveniles (e.g., lizards,
caterpillars, plants).
The second objective of the symposium
was to explore the diversity of maternal effects other than those mediated through
propagule size. Propagule size is an obvious
candidate maternal phenotype that can af-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
85
feet offspring phenotypes, it is highly vari- ecologists on maternal effects as a potenable at many levels in nature, and it has tially significant (i.e., of statistically large
rightly received tremendous attention from effect) and meaningful (i.e., w. r. t. fitness)
both theoretical and empirical evolutionary source of variation in early offspring sucecologists (Bernardo, 1996). Yet, there are cess, (2) to suggest how maternal effects are
many other avenues for maternal effects be- relevant to the design, analysis and intersides those occurring via propagule size pretation of ecological studies concerning
{e.g., transmission of active gene products juvenile growth and performance, whether
during post-ovulatory fetal nutrition; effects or not maternal effects per se are of interest
mediated through maternal behavior), and to the investigator, (3) to highlight fruitful
all maternal effects can impact offspring fit- areas for future research and review, and (4)
ness. Many of these other maternal effects to identify areas in which research momenare also highly relevant to ecological stud- tum or implicit assumptions impede reies, but have not been given as much atten- search activity or perspectives. Space contion from ecologists as has propagule size. straints preclude a comprehensive review.
The last principal goal of the symposium Indeed, several topics discussed here each
was to illustrate that the magnitude or im- merits careful review (e.g., effects of egg
portance of a maternal effect is often likely size in animals; oviposition site choice as a
to be contingent on many other facets of an general problem). Rather, I try to identify
offspring's environment. Indeed, a single open questions and implicit assumptions in
maternal decision can have diverse impli- both theoretical and empirical work, and to
cations. Consider a mother's choice of ovi- overview summary literature as a solid baposition sites. Mothers can discriminate sis for future work.
among sites based on characteristics rangMaternal effects in animals versus plants:
ing from temperature and moisture regimes This paper (like the symposium) emphasizto food quality and potential levels of com- es empirical work in animal systems, alpetition that offspring are likely to experi- though many (but not all) of the issues disence, and variation in these aspects of off- cussed apply as much to plant systems. This
spring environments affects offspring per- bias is warranted on several grounds. First,
formance (below). In other words, it is nec- ecological botanists seem to be generally
essary to study maternal effects within an more aware that maternal effects impinge
ecological context, for this context not only on variables like seed size that are relevant
may contribute to the maternal effect itself to their research, perhaps because seed size
(e.g., effects of resource environment on is both a common response variable in studmaternal egg size) but environments inter- ies of adult fitness, and a prominent source
act with, and possibly modify the expres- of variation in seedling performance (resion of maternal effects as they impinge views: Roach and Wulff, 1987; Lacey,
upon offspring fitness.
1991). Second, there exists a clear bias in
In this paper I overview the underex- at least the perception of relevant work in
plored role of maternal effects in ecological animal systems. For example, in a review
research, elaborating upon the three themes and model of the familiar issue of optimal
that comprised the objectives of the sym- propagule size, McGinley et al. (1987) proposium. First, I identify a working defini- vide extensive review of research in plants,
tion that broadly encompasses the diversity but cursory coverage of relevant work in
of elements that constitute maternal effects. animals beyond that attributable to differI then survey this maternal effects diversity. ences in amount of research that had been
In this survey, I pay particular attention to conducted in both groups when their paper
topics other than propagule size research was written. Finally and perhaps most im(see Bernardo, 1996). I conclude by de- portantly, as is true with many evolutionary
scribing some of the ecological and evolu- and ecological problems, the behavioral
tionary implications of maternal effects that complexities and motility of animals allow
are germane to ecology. My goals for the if not require different functional relationpaper are (1) to focus attention of empirical ships between characters than exist in plants
86
JOSEPH BERNARDO
(e.g., Wilbur, 1977). Again, many animal
mothers explicitly choose where to place
their propagules, and these behavioral decisions have demonstrable effects on offspring performance (reviewed below). The
best that a plant mother can do is to adjust
her seed size or structures associated with
seeds to affect their probabilities of dispersal. This diversity of opportunities for
differences between how plants and animals
solve similar ecological problems appears
to be generally underappreciated (e.g.,
McGinley et al., 1987).
Having emphasized reasons for segregation, there are many problems in maternal
effects research common to both plants and
animals, and for some topics I cite results
from both fields to emphasize these similarities. Bridge-building between evolutionary-ecological botanists and zoologists is
needed in many fields (e.g., Arnold,
\994b). However, maternal effects research
is hardly a cohesive problem for zoologists
and this integration is needed before attempting generalizations across larger
realms; perhaps a review of maternal effects
in animal systems might make subsequent
connections more fruitful.
WHAT ARE MATERNAL EFFECTS?
The literature on maternal effects is
abundant and diverse, as are recent reviews
of maternal effects in specific contexts. Students of maternal effects would be wellserved by studying these excellent reviews
because they provide both access to literature on a variety of taxa and topics, and
discussions of general issues concerning
maternal effects (overviews: Kirkpatrick
and Lande, 1989; Riska, 1991; theory:
Cheverud, 1984; Riska et al., 1985; Kirkpatrick and Lande, 1989; Lande and Price,
1989; Riska, 1989; Lande and Kirkpatrick,
1990; Cowley and Atchley, 1992; reviews:
Arnold, 1994a; Cheverud and Moore, 1994;
empirical reviews, plants: Roach and
Wulff, 1987; McGinley et al., 1987; Haig
and Westoby, 1988; Lacey, 1991; insects:
Lees, 1979; Mousseau and Dingle, 1991a,
b; fish: Reznick, 1991; mammals: Cowley,
1991a; development: Cohen, 1979; Newth
and Balls, 1979; behavior: Cheverud and
Moore, 1994).
Conceptual definitions
A concise general definition of a maternal effect is that effect which occurs when
a mother's phenotype directly affects the
phenotype of her offspring (after Arnold,
1994a, p. 36). A maternal effect then is a
part of an offspring's phenotype that does
not result from the action of its own genes
and the interactions of those genes with its
environment. The term "maternal" traces
to pronounced patterns of covariation seen
between maternal nutrition and offspring
size in mammals, the systems in which this
kind of phenotypic transmission was first
extensively recognized and studied. Consequently, mammals have been the model
systems for much maternal effects research,
and thus have provided most of our current
insights into general issues concerning maternal effects (Cheverud, 1984; Riska et al.,
1985; reviews: Newth and Balls, 1979;
Cowley, 1991a; Cheverud and Moore,
1994).
Two points need to be emphasized in defining maternal effects. First, it is important
to recognize that this kind of direct phenotypic effect of parents on offspring phenotypes is not restricted to mothers; fathers'
phenotypes, too, can have these direct effects on offspring phenotypes (Giesel,
1988). This is true when fathers give care
to offspring (as in many birds, mammals
and fish, some frogs; see Clutton-Brock,
1991), when fathers actually make a nutritional investment via copulatory gifts or nutrients transmitted in the spermatophore that
are mobilized by females for egg production (e.g., Nisbet, 1973; Gwynne, 1984;
Markow and Ankney, 1984; Butlin et al.,
1987 and papers cited therein), or if a father's phenotype affects the characteristics of
an oviposition site (either via defense of a
territory, or because of his nest-building
skills) which in turn affects offspring fitness
(e.g., Howard, 1978). The terms "parental
effects" (e.g., Lacey, 1991; Giesel, 1988;
Carriere, 1994; models: Arnold, 1994a) or
more generally, "kin effects" (Willham,
1963, 1972; Cheverud, 1984) are often used
to reflect this more general class of effects.
Nevertheless, as Cheverud and Moore
(1994) emphasized, the term maternal ef-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
87
fects is established in the literature and so maternal effects remains evident in Falcois the term that I use herein. It is also im- ner's definition (1989, p. 137): "prenatal
portant to note that some authors use "pa- and postnatal influences, mainly nutritional,
ternal effects" to mean nuclear genetic ef- of the mother on her young." Despite this
fects of fathers (e.g., Woodward, 1986, emphasis, insights from earlier quantitative
1987; Schmitt and Antonovics, 1986; An- genetic work clearly indicated that maternal
dersson, 1990). This term is not analogous effects, even in viviparous organisms, arise
to "maternal effects" with respect to which from many avenues besides nutritional effects. Cohen (1979) attempts a comprehenvariance component is being described.
With these terminological issues in mind, sive summary of maternal effects, largely
maternal effects are defined more generally from the perspective of developmental pheas a direct effect of a parent's phenotype nomena in offspring. Mather and Jinks
(1971, p. 293) offered this succinct sumon the phenotype of its offspring.
Some authors (e.g., Mousseau and Din- mary:
gle, 1991ft; Rossiter, 1991a; Carriere, 1994)
"Maternal effects arise where the mother
distinguish the case in which a parental makes a contribution to the phenotype of
phenotype affects the same phenotype in her progeny over and above that which rethe progeny from the case in which there is sults from the genes she contributes to the
no obvious phenotype of parents that af- zygote. These contributions may take one
fects progeny phenotypes, but in which or more of the following forms: (i) Cytothere remains evidence of some effect of plasmic inheritance, (ii) Maternal nutrition
parents (e.g., parental photoperiod: Giesel, either via the egg or via pre- and post-natal
1988; Horton and Stetson, 1992). This dis- supplies of food, (iii) transmission of pathotinction has been made apparently because gens and antibodies through the pre-natal
in some cases, it has not been possible to blood supply or by post-natal feeding, (iv)
identify a specific phenotype (a measurable imitative behavior, (v) interaction between
character) of parents that correlates with the sibs either directly with one another or
phenotypic effect seen in offspring. How- through the mother."
ever, such effects remain attributable to paIn summary, even in situations in which
rental phenotypes: They are not contained maternal effects may be largely or obviousin parental genes (e.g., photoperiod), but ly nutritional in nature, there remains the
their transmission to offspring must be ac- potential for non-nutritional maternal efcomplished via the parental phenotype. fects as well.
This means that the distinction is a perceptual artifact (difficulty in identifying a mea- Maternal effects as cross-generation
surable character in parents that is correlat- phenotypic plasticity
ed with the offspring response), rather than
Maternal effects are sometimes interpreta conceptual distinction.
ed as an important mechanism that allows
A second key point about maternal ef- a (presumably adaptive) phenotypic refects is that while nutritionally-mediated sponse in offspring to an environmental cue
maternal effects are clearly widespread, perceived by the parents. In other words,
well-studied, and ecologically important, mothers might adjust the phenotypes of
non-nutritional maternal effects are also di- their offspring in response to cues, perverse and significant in the ecology of early ceived by the mother, about the environstages. Animal breeders were the first to ex- ment her offspring will encounter, in a way
tensively explore maternal effects, and the that enhances offspring fitness. This interfirst to realize that such effects had signif- pretation has been made mostly by botaicant implications for breeding programs: nists and insect workers (reviews: Roach
Large mothers typically produced large off- and Wulff, 1987; Lacey, 1991; Mousseau
spring, but this part of the resemblance was and Dingle, 1991a, b). For example, in reattributable to nutritional effects of mothers. sponse to photoperiod, insects may adjust
Thus nutritional effects were widely stud- reproductive timing, per-propagule investied, and that influence in thinking about ment, and other characters in ways that en-
88
JOSEPH BERNARDO
hance offspring performance (Mousseau
and Dingle, 1991a, b).
Great care must be exercised when thinking about maternal effects as adaptive plasticity. One reason is that, although plasticity
is one of evolutionary biology's most important concepts and phenomena, the term
itself is perhaps the least clearly defined in
the field. Some workers use it to mean "all
phenotypic variance," others mean by it
only "phenotypic variation in response to a
particular environmental variable," still
others use it to mean "genetic variability"
and finally, many workers implicitly treat
plasticity as an intrinsically adaptive phenomenon (discussions in Newman, 1992
and papers therein; Bernardo, 1993, 1994a;
Higgins and Rankin, 1996). The lack of
consensus about the meaning and use of
"plasticity" and its strongly adaptive connotation mean that maternal effects should
be cautiously viewed as a form of plasticity.
Moreover, while many maternal effects are
indeed adaptive, some are not (e.g., transfer
of pathogens across placentae; see also Beeman et al., 1992) and adaptiveness ought
not be assumed, even implicitly, in a general discussion of maternal effects. Finally,
the growing awareness that maternal effects
can have a heritable basis means that their
interpretation as plasticity is a hypothesis
that must be evaluated rather than assumed.
The definition offered above avoids subjectivity of interpretation because it does not
define maternal effects (a phenomenon) in
an adaptive context (a causal hypothesis).
Distinguishing maternal influences:
Maternal selection and maternal
inheritance
Kirkpatrick and Lande (1989) separated
maternal effects into two classes: those that
represent non-Mendelian phenotypic transmission (e.g., size of mother affecting size
of offspring), called "maternal inheritance," and those in which parents actually
exert selection on offspring that is independent of offspring phenotypes (e.g., maternal
defense of her clutch against predators),
called "maternal selection." Specifically,
they state "Maternal inheritance arises
when mothers affect the phenotypes of their
offspring through various non-Mendelian
mechanisms. . . . Maternal selection, on the
other hand, can occur whether or not there
is maternal inheritance. It arises when offspring fitness is directly affected by its
mother's phenotype (holding the effect of
the offspring's own phenotype on its fitness
constant)" (Kirkpatrick and Lande, 1992, p.
284).
Examples of maternal selection include
active defense of the nest or offspring
against predators, distractive behaviors that
deter predation, parental manipulation of
the nest environment (gas exchange, waste
removal, thermoregulation, etc.) that affects
embryo survival, or feeding of the young
to the extent that offspring would not survive without such feeding. Maternal rescue
of genetically defective progeny via transfer
of bioactive peptides (Letterio et al., 1994)
or even transmission of antibodies and other forms of pathogen resistance are perhaps
less obvious examples of maternal selection. Maternal inheritance is evident in features such as amount and quality of propagule nutriments (yolk, endosperm, milk,
etc.), characteristics of the nest arising from
maternal oviposition site choice decisions
that affect offspring growth and survival,
behaviors such as learning (e.g., prey capturing technique) that might affect offspring
growth, etc.
Maternal selection can produce evolutionarily meaningful variation among offspring within a population which affects the
evolutionary dynamics of traits subject to
such selection. One reason is that phenotypic variation among parents in the extent
of maternal selection can produce variation
in fitness. For example, if mothers vary in
their ability to guard nests or young or divert predators with distractive behavior, maternal selection will act as a kind of nonrandom filter through which other kinds of
selection (e.g., predation) are able to affect
offspring, producing variation in offspring
fitness. Thus, when maternal selection occurs, selection on offspring phenotypes is a
joint function of their own genotypes and
their parents' genotypes, because parental
genes influence both progeny phenotypes
(through heredity) and selection on those
phenotypes (via parental behavior). In contrast, although phenotypes of traits subject
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
to maternal inheritance vary as a function
of maternal phenotypes, the impact of that
variance upon offspring fitness is not dependent on parental phenotypes but is evaluated purely by extrinsic selection.
Statistical definitions
Statistical definitions of maternal effects
arise from the use of breeding designs in
quantitative genetic analyses of trait variation (review in Arnold, 1994a). Controlled
breeding designs are used to produce progeny having a variety of statistically describable relationships to each other and to a set
of parents. For example, half-sib designs, in
which multiple experimental families share
one but not the other parent, or full-sib hybrid families among which maternal parents
differ, are useful designs depending on the
parameters of interest. Breeding designs are
factorial in nature, and so are readily analyzed by Analysis of Variance models.
These analyses produce a partitioning of
observed phenotypic variance in some trait
or traits of offspring, and various sources of
that variance (e.g., 9 parent, 6 parent, 9
parent X 8 parent) are tested for their contribution to total phenotypic variance. The
specific breeding design determines which
variance components can be estimated and
tested; hence, general statistical definitions
of maternal effects cannot be made. Moreover, even when using comparable designs,
the calculations and interpretations of effects critically depend on the structure of
the model used and the type of sums of
squares employed. A good example comes
from a quantitative genetic analysis of embryonic and larval traits in a frog, Pseudacris crucifer (see, e.g., Travis et ai, 1987,
p. 148). Correctly, their interpretations depend upon their use of Type I SS; had they
employed a Type III SS, these interpretations of variance components would differ
substantially. While breeding experiments
have great power to evaluate maternal effects, great care should be exercised in their
design, analysis, and the interpretation of
resultant variance components.
DIVERSITY OF MATERNAL EFFECTS AND
SOME OF THE QUESTIONS THEY RAISE
The potential for existence of maternal
effects is as universal as motherhood; the
89
kinds of maternal effects are also many; and
there can exist simultaneously many avenues of maternal selection and maternal inheritance for an individual mother and her
progeny. Consider the variety of maternal
influences in plethodontid salamanders. In
some species such as Desmognathus ochrophaeus, egg size varies considerably
among mothers, although the implications
of this variance for offspring fitness remain
unexplored (Bernardo, 1994a; Bernardo
and S. Arnold, unpublished). This variation
in egg size occurs at the among species level as well, and has different implications at
that level (Tilley and Bernardo, 1993; Collazo, 1996, and below). Many maternal effects arise after eggs are laid. As in many
salamanders, D. ochrophaeus brood their
clutches until hatching, and shortly thereafter. Clever experiments in a few species
have shown that mothers improve hatching
success via several mechanisms (reviews:
Forester, 1979; Nussbaum, 1985; Horn et
ai, 1990). First, mother's presence both reduces desiccation (Forester, 1984) and deters most clutch predation (Forester, 1979,
1983). Second, females physically manipulate clutches which is thought both to promote gas exchange and to inhibit growth of
fungal mycelia because unattended clutches
succumb to fungal infection and death in a
few days (Forester, 1979; Bernardo, personal observation). Third, mothers also eat
eggs that die and otherwise quickly fungus;
without maternal intervention, these few
dead eggs doom the entire clutch (Forester,
1979). It has also been shown that the collective effects of all of these agencies of
maternal care improve with maternal size
(age), because clutches brooded by larger
females have higher proportional hatching
success than those brooded by smaller females (Horn, 1987). However, because maternal age, size, and egg size covary, the
specific mechanisms by which larger females realize higher hatching success have
not been unambiguously identified. Despite
the fitness gains that mothers realize by
brooding, they are also subject to personal
costs. Attending females do not actively
feed, and they lose mass both to dehydration and tissue loss during brooding (Forester, 1981, 1984). Brooding females are
90
JOSEPH BERNARDO
susceptible to predation by larger vertebrate
predators (Forester, 1979). Conflicting selection on maternal phenotypes thus exists,
and the way in which a balance is struck
between these may relate to the likelihood
of extrinsic mortality (Bernardo, 1994).
This example illustrates the great variety of
issues and questions to be addressed in maternal effects research, some of which I now
survey.
guishes a large class of maternal effects.
However defined, subsets of specializations
associated with "viviparity" are widespread throughout vertebrates {invertebrates: reviewed in Lombardi, 1996; overviews of vertebrate viviparity: Guillette,
1989; Packard et al., 1989; Shine, 1989;
Wake, 1989, 1992; Blackburn, 1992; fish:
Wourms et al., 1988; Kormanik, 1992;
Wourms and Lombardi, 1992; Lombardi,
1996; amphibia: Wake, 1982, 1993; reptiles: Shine and Bull. 1979; Shine, 1983a,
b; Stewart, 1992, 1993; Blackburn, 1993,
1994; lizards: Guillette, 1993; Blackburn,
1982; snakes: Blackburn, 1985; Stewart,
1992; mammals: Cowley, 1991a). Blackburn (1992) counts 132 independent evolutionary inventions of viviparity in
vertebrates. The multiple origins of placentation and other viviparous specializations,
both among major invertebrate and vertebrate clades (Wake, 1989, 1992; Blackburn,
1992; Lombardi, 1996) and within vertebrate clades (above references) suggests its
net adaptive value, and the critical role this
kind of maternal influence has on the early
ecology of juveniles of many kinds. Ecologists have scarcely studied this diversity,
but as the anatomical descriptions and taxonomic extent of specializations continue to
be described, studies of the ecological roles
of viviparity will likely blossom.
Viviparity
Viviparity is a concept that everyone
seems to grasp but that has been challenging to satisfactorily define, because no single set of criteria is universally applicable
among different taxa (discussions in Blackburn, 1992; Wake, 1992; and references
therein). These terminological issues are far
from semantic. Rather, they concern the
types, relative timing, and extent of maternal influence on zygotes or embryos. For
example, many lizard workers interpret
simple egg retention, in which females give
birth to retained eggs without post-ovulatory nutrient exchange, as viviparity solely
because females give birth to live young.
While "parturition of live young" is consistent with the latin origins of viviparity, it
seems misleading to consider egg retention
in the same category as those lizards that
have evolved highly specialized placentalike arrangements {e.g., Mabuya; Blackburn
Nutritional and non-nutritional maternal
et al., 1984). Broad inclusion of egg retain- effects in viviparous taxa.—The energetics
ers in the same category as the eutherian- of lactation and variation among mothers in
like reproductive mode of Mabuya both di- their capacity to sustain lactation are an acminishes the significance of evolutionary tive area of research {e.g., Fuchs 1982; Roinnovations seen in beasts like Mabuya, and gowitz, 1996). In addition to the diversity
serves also to mask another exciting cate- of kinds of transplacental exchange allowed
gory of maternal effects having nothing to by the sympathy of maternal and fetal tisdo with fetal nutrition: Although egg re- sues (carbohydrates, ions, gas exchange,
tainers might seem to have limited oppor- and various combinations) that presumably
tunity for communication between maternal drove the convergent evolution of placentae
and fetal tissues, the retention by mothers and placenta-like arrangements, these strucof embryos still allows transmission of ma- tures allow a variety of non-nutritional maternal influence, for example, via maternal ternal effects as well. Again, these effects
thermoregulatory behaviors. These kinds of are especially well-studied in mammals,
maternal influence are very different from and scarcely if at all in other taxa having
the trophic, hormonal, and immune inter- placental specializations. These effects inactions allowed by placenta-like tissues.
clude transfer of photoperiod information
A cogent, general definition that captures (review: Horton and Stetson, 1992), transfer
all of the flavors of viviparity may be elu- of immunological competence via antibodsive. Nevertheless, "viviparity" distin- ies, transfer of pathogens or toxins, hor-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
monal influence (Clark and Galef, 1995) or
transfer of bioactive peptides that "rescue"
genetically defective progeny (e.g., Letterio
et al., 1994). Some of these factors may
also be transmitted by the mother post-parturitively via milk or other fluids. It should
be emphasized that many maternal effects
transmitted in these ways can be detrimental, as evidenced by birth defects in humans
attributable to substance abuse of mothers.
Non-nutritional maternal effects transmitted
across placentae deserve further study in
non-mammalian viviparous taxa (e.g., discussion in Lombardi, 1996).
It is also noteworthy that mothers that
maintain developing embryos in their bodies, whether truly viviparous or not, can
have other impacts upon their progeny.
Thermoregulatory behavior and photoperiod are some examples of such effects, but
again, these kinds of effects have scarcely
been studied, even in mammals.
Experimental analysis of maternal effects
in viviparous taxa.—Mammalogists have
used an elegant experimental design known
as embryo-transfer in pioneering analyses
of maternal effects in model systems (e.g.,
Riska et al., 1985; Cowley, 1991a, 6).
These techniques have not been widely applied to analysis of maternal effects in natural mammal populations (but see Roth and
Klein, 1986) despite great interest in body
size clines in natural mammal populations
(e.g., Bronson, 1979; Zammuto and Millar,
1985; Dobson and Murie, 1987; Lynch,
1992). The potential for maternal effects in
these systems has been acknowledged
(Roth and Klein, 1986; Dobson and Michener, 1995). The conceptual and logistic
leap from experimental analysis of maternal
effects mediated through body size in the
lab to the field is not great (Roth and Klein,
1986); given that maternal size exerts such
great effect on offspring phenotypes of
small mammals in the lab, it seems likely
that mammalian ecologists interested in
body size, juvenile growth and development, and even population dynamics could
exploit embryo-transfer techniques in field
experiments. Perfection of these techniques
in non-mammalian viviparous taxa will be
a powerful tool for studying placentally
91
transmitted maternal effects upon offspring
fitness in natural populations.
Oviposition site choice
Abundant data from diverse taxa indicate
that mothers do not oviposit their eggs haphazardly. Oviposition site choice has been
widely studied in insects, particularly in
plant-herbivore systems, revealing great
variability and sophistication in maternal
oviposition site choosing behaviors (review: Rausher, 1983a). For example, herbivorous insects can discriminate among
host plants based on plant morphology
(Rausher, 1978), plant density (Rausher,
1980, 19836), plant chemistry (Rausher,
1981a; Feeney et al., 1983), egg load on
potential host plants (Rausher, 1979a), and
multivariate nutritional quality of the plant
(Rausher, 1981a). Oviposition decisions in
turn often affect offspring performance: Effects upon the quality of offspring diet
(Rausher, 1980, 1981a, 1983a), potential
levels of competition or predation that offspring will encounter (Rausher, 1979a; Resetarits and Wilbur, 1989), and offspring
growth or survival (Rausher, 1980; Rausher
and Papaj, 1983; Papaj and Rausher, 1987a;
Singer, 1984; Singer et al., 1988) have been
found (but see Rausher, 19796). If there exist both variation among females in oviposition site discrimination (Rausher, 19816;
Papaj and Rausher, 1983; Roosenburg,
1996) and underlying genetic variation for
those behaviors (Rausher, 19836; Papaj and
Rausher, 19876; Barker et al., 1994) then
selection can mold them in ways that jointly
increase maternal and offspring fitness
(e.g., Mitchell, 1975; Papaj and Rausher,
19876; Ng, 1988; Singer et al., 1988, 1994;
Barker et al., 1994; but see Rausher,
1983c).
Compared to these detailed analyses of
oviposition site choice in insects (including
parisitoids), far less is known about the
ability of non-insect invertebrate and vertebrate mothers to discriminate and respond
to variation among potential oviposition
sites. This is surprising given interest by
vertebrate workers in consequences of abiotic effects for vertebrate eggs (reviews:
Seymour, 1984; Deeming and Ferguson,
1991a, 6 and below). Vertebrate workers
92
JOSEPH BERNARDO
have emphasized effects of variation in abiotic conditions in which eggs develop: Abiotic conditions of the nest influence hatchling sex (Packard and Packard, 1984; Janzen, 1993; Janzen and Paukstis, 1991;
Roosenburg, 1996), size (Packard and
Packard, 1984; Gutzke and Packard, 1987;
Van Damme et al, 1992; Overall, 1994),
locomotory performance (Miller et al.,
1987; Van Damme et al., 1992), subsequent
growth rate (Van Damme et al, 1992;
Overall, 1994) and other aspects of offspring phenotypes (Bradford 1984, 1990;
Packard and Packard, 1984; Congdon and
Gibbons, 1990; Overall, 1994).
There is some work on oviposition site
discrimination in vertebrates. In a field experiment, Resetarits and Wilbur (1989)
found that female frogs (Hyla chrysoscelis)
detect the presence of predators and the
density of conspecific eggs in potential oviposition sites, avoiding them in favor of
sites without predators or the eggs of competitors. Interestingly, female avoidance behavior of these sites occurred despite the
presence of actively calling males in those
sites (Resetarits and Wilbur, 1991). The implications of these female oviposition decisions are clear from numerous other studies of tadpole growth: tadpoles are heavily
preyed upon by fish and salamander predators, and their growth and developmental
rates are highly sensitive to density.
Another example concerns nest site selection in reptiles having temperature-dependent sex determination (TSD; review:
Janzen and Paukstis, 1991). Despite great
interest in studies of the physiological and
genetic basis for TSD, surprisingly little
ecological work has asked whether maternal oviposition behaviors might actively
distinguish among potential nest sites on
the basis of expected nest temperatures (and
hence, on expected sex of hatchlings) in a
way that enhances offspring fitness. Diamondback terrapins (Malaclemys terrapin)
show sexual size dimorphism in which
males are far smaller than females at maturity. There is also substantial variation
among mothers in their egg sizes. Longitudinal data from marked individual terrapins indicated that females with large eggs
are more likely to oviposit those eggs in
microhabitats in which females will be produced (Roosenburg, 1996). Females hatching from these larger eggs attain sexual maturity earlier than females hatching from
smaller eggs. Hence, mothers that can discriminate among nest sites as a function of
both nest site temperature and the size of
eggs that they carry can affect offspring fitness via the differential impact of egg size
on growth rates in the two sexes.
The potential for widespread oviposition
site choice behaviors in vertebrates is a
fruitful area for study (Resetarits, 1996); the
sophisticated literature on oviposition site
choice in insects contains a rich pool of
ideas and designs for exploring analogous
effects in vertebrates and other understudied taxa.
Parental care
Parental care is widespread in animals
(review: Clutton-Brock, 1991). Parents in
many taxa brood eggs or young (e.g., centipedes, scorpions, caecilians, some lizards,
some salamanders, crocodilia) for a multiplicity of reasons (above) unrelated to posthatching or post-parturitive feeding. And
too, many parents feed young after hatching
or birth (mammals, many birds, some anura, some fish). Variation among individuals
in extent and quality of these and other
kinds of parental care translates into variable impacts upon offspring phenotypes,
and hence are fertile ground for ecological
studies of maternal effects. Certainly studies of parental care from the perspective of
maternal effects could move beyond the
taxonomic confines of the birds and mammals to seek generality in studies of invertebrates and ectothermic vertebrates.
Maternal age effects
A poorly explored aspect of maternal effects concerns effects of maternal age per
si. Most evidence of such effects comes
from mammals and birds, in which longterm mark-recapture programs have allowed investigators to seek effects of maternal age on offspring characters. Such
studies provide limited evidence that maternal age affects offspring phenotypes,
even after features correlated with maternal
age (such as birth weight) have been statis-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
tically adjusted. Trends in three-month survival of juvenile great tits (Parus major)
were related to maternal age (Perrins and
Moss, 1974): Young mothers' chicks and
old mothers' chicks had lower survival than
chicks of middle-aged mothers. The effect
in young mothers was attributed to levels
of maternal experience. In kittiwakes (Rissa
tridactyld), Thomas (1983) found age effects in young mothers, but only for females whose clutches contained three eggs.
Older females also produced larger eggs,
and larger eggs result in higher hatching
and fledging success. Bowen et al. (1994)
found that maternal age explained substantial variance in birth mass of harbor seals
(Phoca vitulina) even after accounting for
effects of maternal mass. This effect was
attributed to maternal "reproductive experience," but a specific mechanism was not
postulated. In studies of bighorns (Ovis
canadensis), Jorgenson et al. (1993) hypothesized an impact of maternal age and
size on age at first reproduction of their
daughters, a result observed in other ungulates (see Jorgenson et al., 1993), but
none was found. The extent of these agespecific maternal effects in birds and mammals in which they could be explored because of long-term mark-recapture studies
of individuals suggests that such "experience"-related maternal effects may be more
widespread in other taxa in which longitudinal studies of individuals are seldom conducted (Tinkle, 1979).
Other studies have detected effects of
maternal traits such as body size on brooding behavior in the Desmognathus salamander example, or egg size, that are clearly
correlated with maternal age. For example,
Semlitsch and Gibbons (1990) experimentally evaluated effects of egg size on larval
performance in salamanders. This interesting study analyzed how these effects were
modified depending on larval environments, and also, how long effects persisted
in different environments. However, the
large eggs used in the experiment came
from four-year old mothers, whereas small
eggs were from one-year old mothers. Because effects of maternal age are confounded with egg size differences, the effect of
"egg size" revealed in the experiment can-
93
not be unambiguously attributed to either
maternal age or to egg size (as noted by the
authors). This point is raised to emphasize
that other potentially meaningful kinds of
maternal effects variance may masquerade
as egg size when correlations between egg
size and maternal age exist (e.g., Congdon
and Gibbons, 1987). Experimental designs
to partition such effects may be difficult or
impossible in many cases, for example, if
young females never produce large eggs.
Such potential confounding need be considered in interpreting the results of analyses
of egg size effects in such systems. Allometric engineering (Sinervo and Huey,
1990; Sinervo, 1990; Bernardo, 1991) may
prove useful in this regard, but only if the
phenotypic engineering can successfully
isolate that part of the phenotype of interest,
and not simultaneously alter variables such
as egg composition.
I have alluded to the fact that maternal
age effects (or a lack thereof) cannot be explicitly detected in populations in which individual ages are unknown, but basic demographic analyses of natural populations
are needed to establish age effects on life
history phenotypes, yet are seldom conducted by ecologists (Tinkle, 1980). The reluctance of ecologists to conduct demographic studies probably stems from funding and publication issues. This unfortunate
trend easily explains why age-based maternal effects (e.g., maternal experiential effects) are poorly studied, though they are
probably taxonomically more widespread
than in birds and mammals. The result is a
perceptual gap about the kinds of maternal
effects that appear to be widespread (egg
size effects which are easily studied in the
short-term) versus those that appear to be
uncommon (maternal age effects). Although no relationship was found between
bighorn mothers' ages and the ages at
which their daughters first reproduced, Jorgenson et al. (1993) could not have asked
the question without longitudinal data on
individuals. Artifacts of research effort due
to funding trends or publication rates, such
as a lack of effort in field demographic
studies, should be considered in discussions
or models that seek general patterns of maternal effects evolution. For example, it
94
JOSEPH BERNARDO
would be premature to conclude that maternal age effects mediated through maternal reproductive experience are common
only in endothermic vertebrates—the potential for such effects simply has not been
explored in other groups.
Propagule size
Propagule size is one of the most pervasive and widely-studied maternal effects
that impinge on the ecology of the early life
history. Besides its impact as a maternal effect, evolution of propagule size is also of
interest because it is closely tied to problems in life history evolution and population biology. The enormous literature on
propagule size evolution only peripherally
considers propagule size in the context of
the entire life cycle—might selection on
early offspring phenotypes in some cases
affect, if not drive, the evolution of maternal phenotypes (Bernardo, 1994a)? In a
subsequent paper (Bernardo, 1996) I explore this literature in detail, and I attempt
a critical overview of major issues that have
been pursued in this work with a goal of
improving the conceptual depth and rigor
of future studies of maternal effects mediated through propagule size.
IMPLICATIONS OF MATERNAL EFFECTS IN
ECOLOGICAL RESEARCH
Evolutionary biologists have long recognized the ubiquity of maternal effects and
the need to account for them in their analyses of trait evolution. Although many ecologists are becoming increasingly aware that
maternal effects critically bear on the analysis of ecological problems, (especially
propagule size; review: Bernardo 1996), it
is disconcerting that some ecologists still do
not take account of them in their research
designs and analysis. Moreover, the idea—
still advocated in current articles (e.g., Conover and Schultz, 1995)—that maternal effects must be "washed out" before evaluating the ecological significance of other
traits, is deeply troubling for it diminishes
what may be a critical component of adaptive evolution in the traits ecologists often
study (see discussion in Bernardo, 1994a).
It is not clear that the phenotypes evaluated
once maternal effects are washed out in this
way are realistic phenotypes worthy of interpretation. In this section, I point out
some of the important implications of maternal effects in ecological research, based
in part on results from recent evolutionary
models. I conclude by discussing how maternal effects are relevant to the design and
interpretation of ecological experiments,
even when the investigator is not interested
in maternal effects per se.
Maternal effects in early ontogeny
Many authors have posited a role for maternal effects in early ontogeny as a source
of variation that may lead to speciation.
This is because small magnitude variations
early in growth and developmental trajectories can permanently and dramatically alter those trajectories. For example, egg size
differences often characterize closely related species that differ in subsequent body
size and life history (e.g., Elinson, 1987;
Sinervo and McEdward, 1988; Bruce,
1990; Tilley and Bernardo, 1993; Kohn and
Perron, 1994; Collazo, 1996; McEdward,
1996; and others). This potential role of
maternal effects as a mechanism contributing to speciation deserves further study.
Rates and direction of character evolution
and implications for ecological studies
Evolutionary models of how maternal effects affect evolution of other characters
have only recently been generalized to the
case in which multiple attributes of mothers
affect multiple traits in offspring (Kirkpatrick and Lande, 1989; Cowley and Atchley,
1992). These models reveal surprising evolutionary dynamics of traits subject to maternal effects, namely that maternal effects
may result in lags in evolutionary response
of a trait to selection, and more surprisingly, that maternal effects can cause evolution
in a direction opposite to that favored by
selection. In short, the evolutionary dynamics of traits subject to maternal effects are
dramatically different than when maternal
effects are absent, a result suggested by Falconer's (1965) pioneering empirical work.
The distinction between avenues of maternal influence (maternal selection and maternal inheritance) allows modeling of their
discrete impacts on the rate and direction of
ECOLOGICAL SIGNIRCANCE OF MATERNAL EFFECTS
evolution of a mean phenotype (Kirkpatrick
and Lande, 1989; Lande and Kirkpatrick,
1990), but it also clarifies study of maternal
effects by ecologists. One valuable insight
for ecologists that arises from this distinction is that it emphasizes that both kinds of
maternal influence need not exist simultaneously. Mothers might exert maternal selection via parental care although there is
no maternal inheritance (e.g., Reid and
Boersma, 1990), or the opposite may be
true. In other words, maternal effects may
be occurring via maternal behavior (possible maternal selection) even when the ecologist cannot detect, say, variation among
families in egg size (a kind of maternal inheritance). Consideration of multiple avenues of maternal influence is vital: In this
example, consideration of just propagule
size would mean missing a potentially significant source of maternal influence, and
possibly misinterpreting phenotypic variation in offspring phenotypes.
The intriguing evolutionary dynamics revealed by these models have further implications for understanding the ecological
roles of trait variation, and how ecologists
analyze and interpret short-term experiments. One effect revealed by the models
is that traits subject to maternal inheritance
will cause time lags in population response
to selection on those traits. That is, when
there is maternal inheritance in a trait, response to selection in one generation depends not only on the force of selection in
the current generation, but on both the force
of selection and the evolutionary response
in the previous generation (Kirkpatrick and
Lande, 1989; Lande and Kirkpatrick, 1990;
Cowley and Atchley, 1992). Hence, the value of this distinction for ecologists is that
when attempting to understand sources of
variance (in the statistical sense) in offspring survival, growth, or other phenotypes, or even population dynamics, both
maternal selection and maternal inheritance
are likely to explain parts of total variance,
and experiments can be designed to distinguish these distinct influences (e.g., Rossiter, 1991ft). Moreover, maternal effects
might explain patterns of variation that are
otherwise puzzling (e.g., Janssen et al.,
1988). What this means for ecologists is
95
that the impact on fitness components (survival, growth, reproduction etc.—common
response variables in ecological studies) of
ecological factors as measured in a single
field season or a single generation may have
less to do with fitness than ecologists have
typically assumed. Minimally, this suggests
the importance of multi-year field studies
(Tinkle, 1979) and multi-year experiments
by ecologists when we wish to make evolutionary statements concerning traits that
are subject to maternal inheritance (arguments involving concepts such as fitness,
fitness components, adaptiveness, and so on
based on response variables such as growth
rate, body size, survival and the like). It
also suggests that ecologically based causal
pathways of trait variation that are estimated within a generation may often overestimate the true impact of current ecological
conditions if the trait of interest is subject
to maternal inheritance.
Another important insight from these
models is that, due to time lags in evolutionary response of traits subject to maternal inheritance, it is possible for trait means
to continue to evolve after selection has
ceased ("evolutionary momentum". Kirkpatrick and Lande, 1989; Lande and Kirkpatrick, 1990; see also Reznick, 1981; Riska et al., 1985). Again, the implications of
these results for ecological studies are great;
analyses of phenotypic variation and its impacts upon fitness correlates based upon a
snapshot of a single generation or a single
field season—a common paradigm for ecological studies—simply do not capture the
relevant time scale over which ecological
variables (competition, predation, photoperiod, nutrient levels, etc.) affect fitness
when the traits of interest—often characters
such as body size, growth rates, and reproductive output—are subject to maternal inheritance. As has already been seen, ecologists have amassed substantial data that
show that many such characters are indeed
subject to maternal inheritance, meaning
that this finding is highly relevant to much
ecological research.
Demographic implications
A largely unexplored issue with respect
to maternal effects is their potential impact
96
JOSEPH BERNARDO
on population parameters (but see Schall,
1984; Rossiter, 19916; Bridges and Heppell, 1996). Maternal effects often influence
offspring survival (e.g., Rausher and Papaj,
"1983 and many examples cited above)
which alone suggests their potentially significant effect on demography. But many
demographic parameters are susceptible to
maternal effects variation including age
structure, size structure (via affects on offspring growth rates), sex ratio, and recruitment rates (detailed below) (Rausher and
Papaj, 1983; Rossiter, 1991&; Pontier et al,
1993; Bridges and Heppell, 1996; Roosenburg, 1996; and others). In Malaclemys
(Roosenburg, 1996), patterns of variation
between egg size and characteristics of sites
in which females actually laid their eggs
could clearly affect average population parameters such as sex ratio, ages and sizes
at first reproduction, operational sex ratio,
and cohort generation time. Moreover, that
maternal effects may persist in offspring
until they themselves mature (see below)
indicates the importance of a consideration
of maternal effects on population-level phenomena, as well as the more familiar
among-individual level at which they have
mostly been studied. The ability to pursue
such questions in natural populations requires longitudinal studies of individuals,
both to be able to associate a mother's phenotype with that of her progeny, and then,
to observe the impact of those effects, in
the context of a population of mothers and
their offspring, on population phenomena
(e.g., Roosenburg, 1996). These are complex but tractable problems; it is doubtful
that laboratory approaches to them will
shed much light on how maternal effects act
in nature. However, life tables and population projection models can be exploited to
explore how various kinds of maternal influence could impact demography (e.g.,
Bridges and Heppell, 1996).
Variable expression of maternal effects:
Persistence, contingency and
non-uniformity
Expression of maternal effects may vary
in duration, the way they interact with other
features of the offspring's phenotype or environment, and in which tissues or struc-
tures they are detected. These three kinds
of variation in the expression of maternal
effects are relevant in both ecological and
evolutionary contexts. For example, ecological factors such as resource availability
in juvenile environments may mask maternal nutritional effects that would be apparent in more stressful environments (e.g.,
Marsh, 1986; Semlitsch and Gibbons, 1990;
Miao et al., 1991). This means that the phenotypes of juveniles evaluated by selection
will sometimes reflect maternal effects, and
sometimes will not. When maternal effects
are transparent to selection (that is, when
they contribute relatively little to the phenotypic variance among individuals in a
population), selection on maternal effects is
diffuse compared to when maternal effects
comprise a larger proportion of the total
phenotypic variance among individuals.
Hence, variable expression of maternal effects has implications for both short-term
ecological responses (e.g., juvenile performance), and longer-term evolutionary responses to selection.
Persistence.—One of the most intriguing
properties of maternal effects is that they
transmit environmental and genetic influences through time (Riska et al., 1985; Riska, 1991). Consequently, their duration and
hence, their impact upon offspring phenotypes can vary not just in magnitude (variation among mothers in magnitude of maternal influence) but in the total time over
which the effect is expressed. This attribute
has a variety of implications for both trait
evolution and ecological understanding.
Surprisingly few ecological studies have
assessed how long maternal effects last, but
recent studies that have directly evaluated
the duration of maternal effects indicate that
they can persist late into ontogeny, and
even into subsequent generations. In an
ecological experiment, Semlitsch and Gibbons (1990) found that differences in initial
body size among larval salamanders (Ambystoma talpoideum) (hatched from larger
eggs of older mothers) persisted 49 days but
had disappeared by 129 days. The size differences contributed to differences in early
larval growth rates and hence, survival differences, although the size differences disappeared presumably because of subse-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
quent compensatory growth. In contrast, in
studies of maturation of Daphnia, Ebert
(1993) found that maternal effects mediated
through egg size could still be detected in
juveniles when they themselves matured.
Schluter and Gustafsson (1993) examined
maternal effects in collared flycatchers (Ficedula albicollis) from a longitudinal study
in which maternal phenotype (clutch size)
was experimentally manipulated. They detected effects on the clutch size of daughters in their first breeding attempt (one year
later), and an association between maternal
condition and daughter's clutch size as well.
Miao et al. (1991) studied effects of maternal nutritional environments of Plantago
major on offspring germination success under a variety of ecological conditions for
three generations; they detected P, maternal
effects on F2 progeny. These diverse examples of how maternal effects can persist
in their effects on phenotypes are sobering
for ecologists. At best, failure to consider
that some of the variation among juveniles'
phenotypes can be explained by effects
transmitted from their parents means that
the variation is included in the error of estimates of other treatment effects. At worst,
failure to consider this possibility in the design of ecological studies may produce positively misleading results.
Contingency.—Miao's et al. (1991) creative study illustrates another aspect of variable expression of maternal effects, namely,
their contingency on other features of the
offspring's phenotype and the environments
it encounters. Contingency of expression of
maternal effects is one of the strongest examples of how maternal effects are intimately part of ecological studies of juvenile
performance. Miao et al. found that the expression in the progeny of experimentally
produced maternal effects depended on the
kind of environment in which progeny germinated (high or low competition, nutrient
environment experienced by progeny, and
its life history stage). A variety of studies
of fish and frogs have found that maternal
egg size effects on larval growth, development and survival and metamorphic traits
depended on environmental treatments in
the laboratory {e.g., Berven, 1982; Marsh,
1986; Semlitsch and Gibbons, 1990; Pari-
97
chy and Kaplan, 1992). All of these studies
indicate that a given maternal influence
may or may not impact offspring phenotypes, depending upon juvenile environments. While illuminating, many of these
studies were conducted under laboratory
conditions whose relationship to field conditions was not well-established. This fact
highlights the necessity of studying phenotypes in natural contexts when the goal
of the research is to make statements about
fitness or adaptation. To show an effect of
seed size in the greenhouse, or of egg size
in dish pans in the laboratory, much like the
quantitative genetic analysis of other life
history attributes in the laboratory, provides
weak information at best about the ecological implications of maternal effects. In other words, meaningful inferences about the
ecological significance of maternal effects
will ultimately require a field-oriented approach.
Non-uniformity of expression.—Again
returning to Miao et al.'s study, maternal
effects could be detected in some aspects of
offspring morphology, but not in other features. In a very different study, Cowley
(19916) evaluated maternal effects on a
suite of morphological variables (organ and
fat pad weights) in inbred mice strains using embryo-transfer experiments. He found
that, at later sampling dates, maternal effects could still be detected for some offspring characters, but not others in which
maternal effects had been seen at younger
offspring ages. These results are significant
for ecologists: while maternal effects may
not be evident in some traits that are typically measured, they may be expressed in
other traits that were not considered for
study.
IMPLICATIONS FOR DESIGN OF
ECOLOGICAL STUDIES
Our developing understanding about the
role of maternal effects in both the phenotypic expression and evolution of offspring
traits suggests that failure to consider maternal effects explicitly in ecological studies
of such traits may lead at best, to incomplete explanations of juvenile ecology, and
at worst, to inaccurate interpretations.
Hence, maternal effects are relevant in the
98
JOSEPH BERNARDO
design, analysis and interpretation of ecological studies, whether or not the investigator is interested in maternal effects per se.
end of the experiment might as easily be
caused by biases in the distribution of families (and hence, maternal egg size effects
or genetic differences) across experimental
Accounting for maternal effects when they treatments as by the treatments.
are not the focus of study
There are two obvious alternatives to this
Unfortunately, many ecologists continue common but poor design. The first is simto view maternal effects as an annoying ply to sample far more clutches of eggs so
source of variation that must be eliminated that many families contribute to the hobefore a meaningful experiment can be con- mogenized pool from which experimental
ducted (e.g., Conover and Schultz, 1995; subjects are drawn. This would decrease
discussion in Bernardo, 1994a). Ecologists upon each draw the probability of sampling
have commonly used two methods to do an individual from a family already samthis. One strategy is to ignore the existence pled. A second, perhaps better alternative
of such variation by simply homogenizing would be to maintain the identity of indiamong-family variation. For example, it is viduals (and hence, their family affiliation)
often the case that several clutches of eggs throughout the experiment, and to measure
will be collected for an experiment. Rather attributes of the families (e.g., egg size or
than keep track through the experiment of hatchling size) at the outset of the experifamily identity of each individual, clutches ment. Maintenance of family identity alare placed into a common pool from which lows assessment of whether some families
individuals are drawn at random and allo- performed better, or worse, on average, than
cated to experimental treatments.
other families in response to the experiThere are many serious statistical prob- mental treatments. Even if the investigator
lems with this approach. Suppose that we is not interested in such family effects, the
wish to study effects of different resource ability to account for them statistically
environments on larval growth and devel- means that a cleaner estimate of treatment
opment in a caterpillar or tadpole. If only a effects can be made. Moreover, if the infew families (e.g., <5 families, collected as vestigator collected data such as initial egg
clutches of eggs laid in the field) contribute or hatchling size, not only can family difto the total pool of offspring for an exper- ferences be accounted for, but the magniiment, there could easily be significant dif- tude of those effects in relation to differferences among families in egg size (or for ences in egg size can also be estimated and
that matter, in genetic constitution). Al- partitioned from the variation upon which
though a random sampling procedure is treatment effects will be assayed.
used to allocate individuals among the exOther ecologists have at least acknowlperimental treatments, a random procedure edged the potential for maternal effects in
does not insure that, by chance alone, some their experiments, but have used another
treatments have greater, or lesser represen- procedure to "wash out" the maternal eftation of certain families than other treat- fects before beginning an experiment. Typments. This is because with so few possible ically, parental stock is acquired from field
choices (families) upon each random draw populations and then is allowed to "acclifrom the common pool, successive random mate" for one or more generations in a
draws are quite likely to get an individual common lab or field environment as advofrom the same family as a previous draw cated by Conover and Schultz (1995; see
(in this example, P = .20). Given among- also papers cited in discussion in Bernardo,
family variation in egg size, slight biases 1994a). While this approach seems reasonamong treatments in representation of fam- able, it suffers two difficulties (Bernardo,
ilies would necessarily confound treatment 1994a). First, it treats maternal effects difand genetic constitution with egg size, ferences among populations as a nuisance
meaning that the investigator can neither variable, when they might in fact be a critestimate, nor partition these distinct factors. ical component of differences in offspring
In other words, differences observed at the performance in different environments.
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
Second, the rearing of individuals for one
or more generations in an environment that
is different from the native environment before scoring phenotypes allows for an evolutionary response (non-random survival or
reproduction with respect to genotype) to
the novel environment that cannot be estimated or accounted for in subsequent analyses.
Experimental approaches to detect,
partition and estimate maternal effects
The fact that maternal effects are a component of phenotypic variation means that
in order to understand their distinct effects,
it is necessary to have some way of partitioning variation due to maternal effects
from variation due to other sources. This
complexity means that the explicit study of
maternal effects contributions to phenotypes is a patently experimental problem.
Many experimental approaches can be
used to evaluate the role of maternal effects
in ecological studies. Breeding designs to
isolate maternal effects are straightforward,
although their actual implementation may
be tedious in taxa with long generation
times. However, many species can be studied in the field using breeding designs with
a little creativity on the part of biologists.
Neither researchers nor reviewers should
assume sans reflechir that such studies are
not tractable or valuable, including experiments in taxa whose generation times may
exceed several years. Such experiments
have enormous potential to elucidate how
maternal effects influence offspring performance under natural conditions through
multiple environments (e.g., in different
years for longer-lived taxa), and for a wide
diversity of taxa rather than just poeciliid
fish, Drosophila, a few annual plants and
frogs. Greater species pluralism is needed
in all kinds of life history research, but perhaps no more than in the area of quantitative genetic analyses of life histories (including of maternal effects) under field conditions.
Cross-fostering and embryo-transfer experiments have enormous potential to be
applied to many taxa other than birds and
mammals, respectively. Even within these
taxa, the power of these designs has scarce-
99
ly been tapped to explore ecological phenomena (but see Roth and Klein, 1986). For
example, embryo-transfer experiments in
natural mammal populations would seem a
very powerful tool for evaluating maternal
nutritional effects on offspring performance
when mothers occupy divergent habitats
with very different productivities, say along
elevational clines (e.g., Lynch, 1992; Dobson and Michener, 1995). Similarly, crossfostering designs have typically been applied to clutch manipulation experiments in
birds, and these studies have been very important in understanding the evolution of
clutch size in birds. Even here, some groups
of birds have scarcely been studied, and
others (small songbirds, and to a lesser extent, birds of prey) have been extensively
studied. Relatively few such studies have
actually used cross-fostering designs to separate the effects of parental quality and its
effect on offspring growth etc. from the effects of egg size per se (but see design used
in Reid and Boersma, 1990). Cross-fostering designs can be profitably applied to any
taxa in which a parent broods or cares for
the young, even when feeding is not a
prominent part of the parental care; centipedes, some insects, many fish, frogs, salamanders and lizards would be amenable to
such experiments.
Allometric engineering (review: Bernardo, 1991) can allow experimental reduction
of eggs of older females to make them comparable in size to those of young females,
hence breaking ontogenetic correlation between female age and egg size, and allowing explicit evaluation of maternal age effects as distinct from egg size effects. However, such approaches are not a panacea, for
egg size manipulations implicitly assume
that there are not compositional differences
between eggs of different sizes, which may
often exist (evidence reviewed in Bernardo,
1996).
Factorial designs in field situations are
invaluable for evaluating maternal effects in
ecology in the context of natural environments. Natural environments are an essential part of ecological experiments when the
goal of the research is to make statements
about processes in nature. Such experiments have already been conducted in
100
JOSEPH BERNARDO
many contexts, including for evaluating
classes of maternal behaviors (e.g., oviposition site choice: e.g., Resetarits and Wilbur, 1989; adaptive significance of brooding
behaviors: Forester, 1979) on offspring performance. Importantly, factorial field experiments can be profitably combined with
breeding designs (above), because the latter
are also factorial in nature. This means that
maternal effects (as well as many other specific phenotypic components) can be evaluated in the context of natural environments
that are also factorially manipulated in the
experiment, providing explicit tests of issues such as the contingency of maternal
effects. Factorial field experiments can also
be usefully combined with all the other designs just discussed. For example, a crossfostering study conducted in mothers experiencing different environments would be
a 3-factor experiment.
In advocating experiments, I strongly
echo Roff's (1992) concerns about experimental power and design of experiments
(reviewed in Bernardo, 1994i»). In his example, many of the clutch-size manipulation experiments conducted in birds simply
lack statistical power to detect an effect of
clutch size on fledgling survival (or whatever response variable is of interest). Unfortunately, experiments are often interpreted at face value. Elsewhere (Bernardo,
1996) I discuss how a lack of context for
experimental data, or the use of uncalibrated experimental conditions can result in
dangerous conclusions and interpretations
about egg size variation. Experiments that
are poorly designed (i.e., in which potential
explanatory variables are confounded) or
which lack statistical power are best left undone, for they contribute no understanding
of the phenomenon under study.
CONCLUSIONS AND PROSPECTUS
Maternal effects are diverse and widespread, having been found in most taxa and
for many characters in which they have
been sought. It seems likely that these characters represent a common, effective mechanism for affecting offspring performance
in a variety of ways, especially with respect
to early ecological performance. If true,
maternal effects deserve greater explicit at-
tention from ecologists, both because their
existence may affect experimental designs
directed at other problems, and because maternal effects probably often contribute critically to offspring phenotypes that are of
interest in ecological studies. In this regard,
non-nutritional maternal effects require further scrutiny by ecologists.
Maternal effects do not always have positive effects on offspring phenotypes.
Hence, it is unwise to assume that every
maternal effect is adaptive in some way.
It is encouraging that some maternal effects have received explicit attention from
evolutionary biologists and ecologists.
However, I have suggested that the kinds of
maternal effects that have been extensively
studied, the taxonomic groups in which
most studies have been made, and the kinds
of questions that have been asked are a nonrandom subset of those that exist, reflecting
research artifacts attributable to funding and
publication patterns, historical thinking
about the field, and the kinds of characters
that are easily accessible for study. As several workers have previously noted, maternal effects are probably far more widespread and complex than we currently appreciate, and at least some of our current
perceptions about these effects are affected
by our research programs (Reznick, 1991;
Lacey, 1991). We now appreciate the greater complexity that results from maternal effects which means that ecologists can no
longer ignore maternal effects in their
thinking, in their experimental designs, and
in their interpretations of data.
ACKNOWLEDGMENTS
I thank S. Arnold for invaluable discussions about maternal effects, particularly
with respect to genetic and evolutionary issues. I especially thank the Duke University
Zoology Department, and H. F. Nijhout and
D. Meddock in particular, for providing
limited but essential funds that supported
organization of this symposium. Development of many of the ideas presented here
was supported by grants from NSF (BSR
90-01587, DEB 94-07844), the Highlands
Biological Station, and the Cocos Foundation (Training Grant in Morphology). The
manuscript was completed under the sup-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
port of an NSF/A. P. Sloan Foundation Fellowship for Molecular Evolution (BIR-9411048). This paper is for all the world's
mothers—of all species, past, present and
future—thanks.
REFERENCES
Anderson, S. 1990. Paternal effects on seed size in a
population of Crepis tectorum (Asteraceae). Oikos
59:3-8.
Arnold, S. J. 1992. Constraints on phenotypic evolution. Amer. Nat. 140:S85-S107.
Arnold, S. J. 1994a. Multivariate inheritance and evolution: A review of concepts. In C. R. B. Boake
(ed.), Quantitative genetic studies of behavioral
evolution, pp. 17-48. University of Chicago Press.
Arnold, S. J. 1994b. Is there a unifying concept of
sexual selection that applies to both plants and
animals? Amer. Nat. 144:S1-S12.
Barker, J. S. E, W. T. Starmer, and J. C. Fogleman.
1994. Genotype-specific habitat selection for oviposition sites in the cactophilic species Drosophila buzzatii. Heredity 72:384-395.
Beeman, R. W., K. S. Friesen, and R. E. Denell. 1992.
Maternal-effect selfish genes in flour beetles. Science 256:89-92.
Bernardo, J. 1991. Manipulating egg size to study maternal effects on offspring traits. Trends Ecol.
Evol. 6:1-2.
Bernardo, J. 1993. Determinants of maturation in animals. Trends Ecol. Evol. 8:166-173.
Bernardo, J. 1994a. Experimental analysis of allocation in two divergent, natural salamander populations. Amer. Nat. 143:14-38.
Bernardo, J. 19946. Life history deja vu. Syst. Biol.
43:139-148.
Bernardo, J. 1996. The particular maternal effect of
propagule size, especially egg size: Patterns, models, quality of evidence and interpretations. Amer.
Zool. 36:216-236.
Berven, K. A. 1982. The genetic basis of altitudinal
variation in the wood frog Rana sylvatica. II. An
experimental analysis of larval development. Oecologia 52:360-369.
Blackburn, D. G. 1982. Evolutionary origins of viviparity in the Reptilia. I. Sauria. Amphibia-Reptilia 3:185-205.
Blackburn, D. G. 1985. Evolutionary origins of viviparity in the Reptilia. II. Serpentes, Amphisbaenia, and Ichthyosauria. Amphibia-Reptilia 5:
259-291.
Blackburn, D. G. 1992. Convergent evolution of viviparity, matrotrophy, and specializations for fetal
nutrition in reptiles and other vertebrates. Amer.
Zool. 32:313-321.
Blackburn, D. G. 1993. Standardized criteria for the
recognition of reproductive modes in squamate
reptiles. Herpetologica 49:118-132.
Blackburn, D. G. 1994. Standardized criteria for the
recognition of embryonic nutritional patterns in
squamate reptiles. Copeia 1994:925-935.
Blackburn, D. G., L. J. Vitt, and C. A. Beuchat. 1984.
Eutherian-like reproductive specializations in a vi-
101
viparous reptile. Proc. Natl. Acad. Sci. U.S.A. 81:
4860-4863.
Bowen, W. D., O. T. Oftedal, D. J. Boness, and S. J.
Iverson. 1994. The effect of maternal age and
other factors in birth mass in the harbor seal. Can.
J. Zool. 72:8-14.
Bradford, D. F. 1984. Physiological features of embryonic development in terrestrially-breeding
plethodontid salamanders. In R. S. Seymour (ed.),
Respiration and metabolism of embryonic vertebrates, pp. 87-98. D. W. Junk, London.
Bradford, D. F. 1990. Incubation time and rate of embryonic development in amphibians: The influence of ovum size, temperature, and reproductive
mode. Physiol. Zool. 63:1157-1180.
Bridges, T. S. and S. Heppell. 1996. Fitness consequences of maternal effects in Slreblospio benedicti (Annelida: Polychaeta). Amer. Zool. 36:132—
146.
Brockelman, W. Y. 1975. Competition, the fitness of
offspring, and optimal clutch size. Amer. Nat. 109:
677-699.
Bronson, M. T. 1979. Altitudinal variation in the life
history of the golden-mantled ground squirrel
(Spremophilus lateralis). Ecology 60:272-279.
Bruce, R. C. 1990. An explanation for differences in
body size between two desmognathine salamanders. Copeia 1990:1-9.
Butlin, R. K., C. W. Woodhatch, and G. M. Hewitt.
1987. Male spermatophore investment increases
female fecundity in a grasshopper. Evolution 41:
221-225.
Carriere, Y. 1994. Evolution of phenotypic variance:
non-Mendelian parental influences on phenotypic
and genotypic components of life-history traits in
a generalist herbivore. Heredity 72:420—430.
Chambers, R. C. and W. C. Leggett. 1996. Maternal
influences on variation in egg sizes, in temperate
marine fishes. Amer. Zool. 36:180-196.
Cheverud, J. M. 1984. Evolution by kin selection: A
quantitative genetic model illustrated by maternal
performance in mice. Evolution 38:766-777.
Cheverud, J. M. and A. J. Moore. 1994. Quantitative
genetics and the role of the environment provided
by relatives in behavioral evolution. In C. R. B.
Boake (ed.), Quantitative genetic studies of behavioral evolution, pp. 67—100. University of Chicago Press.
Clark, M. M. and B. G. Galef. 1995. Prenatal influences on reproductive life history strategies.
Trends Ecol. Evol. 10:151-152.
Clutton-Brock, T. H. 1991. The evolution of parental
care. Princeton University Press.
Cohen, J. 1979. Maternal constraints in development.
In D. R. Newth and M. Balls (eds.), Maternal effects in development, pp. 1-28. Cambridge University Press.
Collazo, A. 1996. Evolutionary correlations between
early development and life history in plethodontid
salamanders and teleost fishes. Amer. Zool. 36:
116-131.
Congdon, J. D. and J. W. Gibbons. 1987. Morphological constraint on egg size: A challenge to optimal
102
JOSEPH BERNARDO
egg size theory? Proc. Natl. Acad. Sci. U.S.A. 84:
4145-4147.
Congdon, J. D. and J. W. Gibbons. 1990. Turtle eggs:
Their ecology and evolution. In J. W. Gibbons
(ed.), Life history and ecology of the slider turtle,
pp. 109-123. Smithsonian Institution Press, Washington, D.C.
Conover, D. O. and E. T. Schultz. 1995. Phenotypic
similarity and the evolutionary significance of
countergradient variation. Trends Ecol. Evol. 10:
248-252.
Cowley, D. E. 1991a. Prenatal effects on mammalian
growth: embryo transfer results. 4th ICSEB Proceedings, Vol. II., pp. 762-779, Dioscorides Press
Portland, Oregon.
Cowley, D. E. \99\b. Genetic prenatal maternal effects on organ size in mice and their potential contribution to evolution. J. Evol. Biol. 3:363-381.
Cowley, D. E. and W. R. Atchley. 1992. Quantitative
genetic models for development, epigenetic selection, and phenotypic evolution. Evolution 46:495518.
Deeming, D. C. and M. W. J. Ferguson. 1991a. Egg
incubation: Its effects on embryonic development
in birds and reptiles. Cambridge Univ. Press.
Deeming, D. C. and M. W. J. Ferguson, \99\b. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In D.
C. Deeming and M. W. J. Ferguson (eds.), Egg
incubation: Its effects on embryonic development
in birds and reptiles, pp. 147—171. Cambridge
University Press.
Dobson, F. S. and J. O. Murie. 1987. Interpretation of
intraspecific life history patterns: Evidence from
Columbian ground squirrels. Amer. Nat. 129:382397.
Dobson, F. S. and G. R. Michener. 1995. Maternal
traits and reproduction in Richardson's ground
squirrels. Ecology 76:851-862.
Ebert, D. 1993. The effect of size at birth, maturation
threshold, and genetic differences on the life-history of Daphnia magna. Oecologia 86:243-250.
Elinson, R. P. 1987. Change in developmental patterns: Embryos of amphibians with large eggs. In
R. A. Raff and E. C. Raff (eds.), Development as
an evolutionary process, pp. 1—21. Alan R. Liss,
Inc., New York.
Falconer, D. 1965. Maternal effects and selection response. In S. J. Geerts (ed.), Proc. XI Internal
Congr. Genetics, pp. 763—774, Vol. 3. Pergamon,
Oxford.
Falconer, D. S. 1989. Introduction to quantitative genetics, 3rd ed. Wiley and Sons, New York.
Feeny, P., L. Rosenberry, and M. Carter. 1983. Chemical aspects of oviposition behavior in butterflies.
In S. Ahmad (ed.). Herbivorous insects: Hostseeking behavior and mechanisms, pp. 11—Id. Academic Press, New York.
Forester, D. C. 1979. The adaptiveness of parental
care in Desmognathus ochrophaeus (Urodela:
Plethodontidae). Copeia 1979:332-341.
Forester, D. C. 1981. Parental care in the salamander
Desmognathus ochrophaeus: Female activity pattern and trophic behavior. J. Herpetol. 15:29—34.
Forester, D. C. 1983. Duration of the brooding period
in the mountain dusky salamander (Desmognathus
ochrophaeus) and its influence on agression toward conspecifics. Copeia 1983:1098-1101.
Forester, D. C. 1984. Brooding behavior by the mountain dusky salamander: Can the female's presence
reduce desiccation? Herpetologica 40:105-109.
Fuchs, S. 1982. Optimality of parental investment:
The influence of nursing on reproductive success
of mother and female young house mice. Behav.
Ecol. Sociobiol. 10:39-51.
Giesel, J. T. 1988. Effects of parental photoperiod on
development time and density sensitivity of progeny in Drosophila melanogaster. Evolution 42:
1348-1350.
Guillette, L. J., Jr. 1989. The evolution of vertebrate
viviparity: Morphological modifications and endocrine control. In D. B. Wake and G. Roth (eds.),
Complex organismal functions: Integration and
evolution in vertebrates, pp. 219—233. Wiley and
Sons, New York.
Guillette, L. J., Jr. 1993. The evolution of vivparity in
lizards. Bioscience 43:742—751.
Gutzke, W. H. N. and G. C. Packard. 1987. Influence
of the hydric and thermal environments on eggs
and hatchlings of bull snakes Pituophis melanoleucus. Physiol. Zool. 60:9-17.
Gwynne, D. T. 1984. Courtship feeding increases female reproductive success in bushcrickets. Nature
307:361-363.
Haig, D. and M. Westoby. 1988. Inclusive fitness,
seed resources, and maternal care. In J. L. Doust
and L. L. Doust (eds.), Plant reproductive ecology: Patterns and strategies, pp. 60-79. Oxford
University Press, New York.
Higgins, L. E. and M. A. Rankin. 1996. Different
pathways in arthropod post-embryonic development. Evolution. 50:573-582.
Horn, C. L. 1987. Reproductive ecology of female
dusky salamander, Desmognathus fuscus (Plethodontidae) in the southern Appalachians. Copeia
1987:768-777.
Horn, C. L., N. H. Willets, and C. W. Clark. 1990.
Fitness consequences of nest defense in plethodontid salamanders: Predictions of a dynamic optimization model. Herpetologica 46:304—319.
Horton, T. H. and M. H. Stetson. 1992. Maternal
transfer of photoperiodic information in rodents.
Anim. Reprod. Sci. 30:29-44.
Howard, R. D. 1978. The influence of male-defended
oviposition sites on early embryo mortality in
bullfrogs. Ecology 59:789-798.
Janssen, G. M., G. De Jong, E. N. G. Joosse, and W.
Scharloo. 1988. A negative maternal effect in
springtails. Evolution 42:828-834.
Janzen, F. J. 1993. An experimental analysis of natural
selection on body size of hatchling turtles. Ecology 74:332-341.
Janzen, F. J. and G. L. Paukstis. 1991. Environmental
sex determination in reptiles: Ecology, evolution
and experimental design. Quart. Rev. Biol. 66:
149-179.
Jorgenson, J. T, M. Festa-Bianchet, M. Lucherini, and
W. D. Wishart. 1993. Effects of body size, pop-
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
ulation density, and maternal characteristics on
age at first reproduction in bighorn ewes. Can. J.
Zool. 71:2509-2517.
Kirkpatrick, M. and R. Lande. 1989. The evolution of
maternal characters. Evolution 43:485-503.
Kirkpatrick, M. and R. Lande. 1992. The evolution of
maternal characters: errata. Evolution 46:284.
Kohn, A. J. and F. E. Perron. 1994. Life history and
biogeography: Patterns in Conus. Oxford University Press, New York.
Kormanik, G. A. 1992. Ion and osmoregulation in
prenatal elasmobranchs: Evolutionary implications. Amer. Zool. 32:294-302.
Lacey, E. P. 1991. Parental effects on life-history traits
in plants. 4th ICSEB Proceedings, Vol. II, pp.
735—744. Dioscorides Press, Portland, Oregon.
Lande, R. and M. Kirkpatrick. 1990. Selection response in traits with maternal inheritance. Genet.
Res. 55:189-197.
Lande, R. and T. Price. 1989. Genetic correlations and
maternal effects coefficients obtained from offspring-parent regression. Genetics 122:915—922.
Lees, A. D. 1979. The maternal environment and the
control of morphogenesis in insects. In D. R.
Newth and M. Balls (eds.), Maternal effects in
development, pp. 1-28. Cambridge Univ. Press.
Letterio, J. J., A. G. Geiser, A. B. Kulkarni, N. S.
Roche, M. B. Sporn, and A. B. Roberts. 1994.
Maternal rescue of transforming growth factor-p}l
null mice. Science 264:1936-1938.
Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. Amer. Nat. 141:517-536.
Lombardi, J. 1996. Postzygotic maternal influences
and the maternal-embryonic relationship of viviparous fishes. Amer. Zool. 36:106-1 15.
Lynch, C. B. 1992. Clinal variation in cold adaptation
in Mus domesticus: Verification of predictions
from laboratory populations. Amer. Nat. 139:
1219-1236.
Markow, T. A. and P. F Ankney. 1984. Drosophila
males contribute to oogenesis in a multiple mating
species. Science 224:302-303.
Marsh, E. 1986. Effects of egg size on offspring fitness and maternal fecundity in the orangethroat
darter, Etheostoma specaiabile (Pisces: Percidae).
Copeia 1986:18-30.
Mather, K. and J. L. Jinks. 1971. Biometrical genetics.
Chapman and Hall, New York.
McEdward, L. R. 1996. Experimental mainpulation of
parental investment in echinoid echinoderms.
Amer. Zool. 36:169-179.
McEdward, L. R. and L. K. Coulter. 1987. Egg volume and energetic content are not correlated
among sibling offspring of starfish: implications
for life-history theory. Evolution 41:914-917.
McEdward, L. R. and D. A. Janies. 1993. Life cycle
evlution in asteroids: What is a larva? Biol. Bull.
184:255-268.
McGinley, M. A., D. H. Temme, and M. A. Geber.
1987. Parental investment in offspring in variable
environments: theoretical and empirical considerations. Amer. Natur. 130:370-398.
Miao, S. L., F. A. Bazzaz, and R. B. Primack. 1991.
103
Persistence of maternal nutrient effects in Plantago major. The third generation. Ecology 72:
1634-1642.
Miller, K., G. C. Packard, and M. J. Packard. 1987.
Hydric conditions during incubation influence locomotor performance of hatchling snapping turtles. J. Exp. Biol. 127:401-412.
Mitchell, R. 1975. The evolution of oviposition tactics
in the bean weevil, Callosobrunchus maculatus
(E). Ecology 56:696-702.
Mousseau, T. A. and H. Dingle. 1991a. Maternal effects in insects: Examples, constraints and geographic variation. 4th ICSEB Proceedings, Vol. II,
pp. 745-761. Dioscorides Press, Portland, Oregon.
Mousseau, T. A. and H. Dingle. 19916. Maternal effects in insect life histories. Annu. Rev. Entomol.
36:511-534.
Newman, R. 1992. Adaptive plasticity in amphibian
metamorphosis. Bioscience 42:671—678.
Newth, D. R. and M. Balls. 1979. Maternal effects in
development. Cambridge University Press, New
York.
Ng, D. 1988. A novel level of interactions in plantinsect systems. Nature 334:611—612.
Nisbet, I. C. T. 1973. Courtship-feeding, egg-size and
breeding success in common terns. Nature 241:
141-142.
Nussbaum, R. A. 1985. The evolution of parental care
in salamanders. Misc. Publ. Mus. Zool., Univ.
Michigan 169:1-50.
Overall, K. L. 1994. Lizard egg environments. In L.
J. Vitt and E. R. Pianka (eds.), Lizard ecology:
Historical and experimental perspectives, pp. 51—
72. Princeton University Press.
Packard, G. C. and M. J. Packard. 1984. Coupling of
physiology of embryonic turtles to the hydric environment. In R. S. Seymour (ed.), Respiration
and metabolism of embryonic vertebrates, pp. 99—
119. D. W. Junk Publishers, Boston.
Packard, G. C , R. P. Elinson, J. Gavaud, L. J. Guillette, Jr., J. Lombardi, J. Schindler, R. Shine, H.
C. Tyndale-Biscoe, M. H. Wake, F. D. J. Xavier,
and Z. Yaron. 1989. Group report. How are reproductive systems integrated and how has viviparity evolved. In D. B. Wake and G. Roth (eds.),
Complex organismal functions: Integration and
evolution in vertebrates, pp. 281-293. Wiley and
Sons, New York.
Papaj, D. R. and M. D. Rausher. 1983. Individual
variation in host location by phytophagous insects.
In S. Ahmad (ed.), Herbivorous insects: Hostseeking behavior and mechanaisms, pp. 77—124.
Academic Press, Inc., New York.
Papaj, D. R. and M. D. Rausher. 1987a. Components
of conspecific host discrimination behavior in the
butterfly Battus philenor. Ecology 68:245-253.
Papaj, D. R. and M. D. Rausher. \987b. Genetic differences and phenotypic plasticity as causes of
variation in oviposition preference in Battus philenor. Oecologia 74:24—30.
Parichy, D. M. and R. H. Kaplan. 1992. Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina orientalis. Oecologia 91:579—586.
104
JOSEPH BERNARDO
Perrins, C. M. and D. Moss. 1974. Survival of young
great tits in relation to age of female parent. Ibis
116:220-224.
Pontier, D., J.-M. Gaillard, and D. Allaine. 1993. Maternal investment per offspring and demographic
tactics in placental mammals. Oikos 66:424—430.
Rausher, M. D. 1978. Search image for leaf shape in
a butterfly. Science 200:1071-1073.
Rausher, M. D. 1979a. Egg recognition: its advantage
to a butterfly. Anim. Behav. 27:1034-1040.
Rausher, M. D. 1979b. Larval habitat suitability and
oviposition preference in three related butterflies.
Ecology 60:503-511.
Rausher, M. D. 1980. Host abundance, juvenile survival and oviposition in Battus philenor. Evolution 34:342-355.
Rausher, M. D. 1981a. Host plant selection by Battus
philenor butterflies: The roles of predation, nutrition, and plant chemistry. Ecol. Monogr. 51:1-20.
Rausher, M. D. 1981b. Host plant selection by Battus
philenor butterflies: Evidence for individual differences in foraging behavior. Anim. Behav. 31:
341-347.
Rausher, M. D. 1983a. Ecology of host-selection behavior in phytophagous insects. In R. F. Denno
and M. S. McClure (eds.), Variable plants and
herbivores in natural and managed systems, pp.
223-257. Academic Press, Inc., New York.
Rausher, M. D. 1983ft. Alteration of oviposition behavior by Battus philenor butterflies in response
to variation in host-plant density. Ecology 64:
1028-1034.
Rausher, M. D. 1983c. Conditioning and genetic variation as causes of individual variation in the oviposition behavior of the tortoise beetle, Deloyala
guttata. Anim. Behav. 31:743-747.
Rausher, M. D. and D. R. Papaj. 1983. Demographic
consequences of discrimination among conspecific host plants by Battus philenor butterflies. Ecology 64:1402-1410.
Reid, W. V. and P. D. Boersma. 1990. Parental quality
and selection on egg size in the Magellanic penguin. Evolution 44:1780-1786.
Resitarits, W. J. 1996. Oviposition site choice and life
history evolution. Amer. Zool. 36:205-215.
Resetarits, W. J. and H. M. Wilbur. 1989. Choice of
oviposition site by Hyla chrysoscelis: Role of
predators and competitors. Ecology 70:220-228.
Resetarits, W. J. and H. M. Wilbur. 1991. Calling site
choice by Hyla chrysoscelis: Effect of predators,
competitors, and oviposition sites. Ecology 72:
778-786.
Reznick, D. 1981. "Grandfather effects": The genetics of interpopulation differences in offspring size
in the mosquito fish. Evolution 35:941-953.
Reznick, D. N. 1991. Maternal effects in fish life histories. 4th ICSEB Proceedings, Vol. n, pp. 780793. Dioscorides Press, Portland, Oregon.
Reznick, D., H. Callahan, and R. Llauredo. 1996. Maternal effects on offspring quality in poeciliid fishes. Amer. Zool. 36:000-000.
Riska, B. 1989. Composite traits, selection response,
and evolution. Evolution 43:1172-1191.
Riska, B. 1991. Maternal effects in evolutionary bi-
ology: Introduction to the symposium. 4th ICSEB
Proceedings, Vol. II, pp. 719—724. Dioscorides
Press, Portland, Oregon.
Riska, B., J. J. Rutledge, and W. R. Atchley. 1985.
Covariance between direct and maternal genetic
effects in mice, with a model of persistent environmental influences. Genet. Res. 45:287-297.
Roach, D. A. and R. D. Wulff. 1987. Maternal effects
in plants. Annu. Rev. Ecol. Syst. 18:209-235.
Roff, D. A. 1992. The evolution of life histories: Theory and analysis. Chapman and Hall, New York.
Rogowitz, G. L. 1996. Trade-offs in energy allocation
during lactation. Amer. Zool. 36:197-204.
Roosenburg, W. M. 1996. Maternal condition and nest
site choice: An alternative for the maintenance of
environmental sex determination. Am. Zool. 36:
157-168.
Rossiter, M. C. 1991a. Maternal effects generate variation in life history: Consequences of egg weight
plasticity in the gypsy moth. Functional Ecology
5:386-393.
Rossiter, M. C. 1991b. Environmentally-based maternal effects: A hidden force in insect population
dynamics? Oecologia 87:288-294.
Roth, V. L. and M. S. Klein. 1986. Maternal effects
on body size of large insular Peromyscus maniculatus: Evidence from embryo transfer experiments. J. Mamm. 67:37—45.
Schaal, B. A. 1984. Life-history variation, natural selection, and maternal effects in plant populations.
In R. Dirzo and J. Sarukhan (eds.). Perspectives
on plant population ecology, pp. 188—206. Sinauer, Sunderland, Massachusetts.
Schluter, D. and L. Gustafsson. 1993. Maternal inheritance of condition and clutch size in the collared
flycatcher. Evolution 47:658-667.
Schmitt, J. and J. Antonovics. 1986. Experimental
studies of the evolutionary significance of sexual
reproduction. III. Maternal and paternal effects
during seedling establishment. Evolution 40:817829.
Semlitsch, R. D. and J. W. Gibbons. 1990. Effects of
egg size on success of larval salamanders in complex aquatic environments. Ecology 71:17891795.
Seymour, R. S. 1984. Respiration and metabolism of
embryonic vertebrates. D. W. Junk Publishers,
Kluwer Academic Press, Boston.
Shine, R. 1983a. Reptilian reproductive modes: The
oviparity-viviparity continuum. Herpetologica 39:
1-8.
Shine, R. 1983b. Reptilian viviparity in cold climates:
Testing the assumptions of an evolutionary hypothesis. Oecologia 57:397-405.
Shine, R. 1989. Ecological influences on the evolution
of vertebrate viviparity. In D. B. Wake and G.
Roth (eds.), Complex organismal functions: Integration and evolution in vertebrates. Wiley and
Sons, New York.
Shine, R. and J. J. Bull. 1979. The evolution of livebearing in lizards and snakes. Amer. Nat. 113:
905-923.
Sinervo, B. 1990. The evolution of maternal investment in lizard;.: An experimental and comparative
ECOLOGICAL SIGNIFICANCE OF MATERNAL EFFECTS
analysis of egg size and its effects on offspring
performance. Evolution 44:279-294.
Sinervo, B. and L. R. McEdward. 1988. Developmental consequences of an evolutionary change in
egg size: An experimental test. Evolution 42:885899.
Sinervo, B. and R. B. Huey. 1990. Allometric engineering: An experimental test of the causes of interpopulational differences in performance. Science 248:1106-1109.
Singer, M. C. 1984. Butterfiy-hostplant relationships:
Host quality, adult choice, and larval success.
Symp. R. Entomol. Soc. Lond. 11:81-88.
Singer, M. C, D. Ng, and C. D. Thomas. 1988. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977-985.
Singer, M. C, C. D. Thomas, H. L. Billington, and C.
Parmesan. 1994. Correlates of speed of evolution
of host preference in a set of twelve populations
of the butterfly Euphydryas editha. Ecoscience 1:
107-114.
Stewart, J. R. 1992. Placental structure and nutritional
provision to embryos in predominantly lecithotrophic viviparous reptiles. Amer. Zool. 32:303312.
Stewart, J. R. 1993. Yolk sac placentation in reptiles:
Structural innovation in a fundamental vertebrate
fetal nutritional system. J. Exper. Zool. 266:431449.
Strathmann, R. R. 1977. Egg size, larval development, and juvenile size in benthic marine invertebrates. Amer. Nat. 111:373-376.
Stathmann, R. R. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Ann. Rev. Ecol. Syst. 16:339—
361.
Stathmann, R. R. 1990. Why life histories evolve differently in the sea. Am. Zool. 30:197-207.
Stathmann, R. R. 1993. Hypotheses on the origin of
marine larvae. Ann. Rev. Ecol. Syst. 24:89-117.
Thomas, C. S. 1983. The relationships between breeding experience, egg volume, and reproductive success of the kittiwake Rissa tridactyla. Ibis 125:
567-574.
Tilley, S. G. and J. Bernardo. 1993. Life history evolution in plethodontid salamanders. Herpetologica
49:154-163.
Tinkle, D. 1979. Long-term field studies. Bioscience
29:717.
Travis, J., S. B. Emerson, and M. Blouin. 1987. A
105
quantitative-genetic analysis of larval life-history
traits in Hyla crucifer. Evolution 41:145-156.
Van Damme, R., D. Bauwens, F. Brana, and R. F. Verheyen. 1992. Incubation temperature differentially affects hatching time, egg survival and hatchling performance in the lizard Podarcis muralis.
Herpetologica 48:220-228.
Wake, M. H. 1982. Diversity within a framework of
constraints. Amphibian reproductive modes. In D.
Mossakowski and G. Roth (eds.), Environmental
adaptation and evolution, pp. 87-106. Gustav Fischer, New York.
Wake, M. H. 1989. Phylogenesis of direct development and viviparity in vertebrates. In D. B. Wake
and G. Roth (eds.), Complex organismal functions: Integration and evolution in vertebrates, pp.
235-250. Wiley and Sons, New York.
Wake, M. H. 1992. Evolutionary scenarios, homology, and convergence of structural specializations
for vertebrate viviparity. Amer. Zool. 32:256-263.
Wake, M. H. 1993. Evolution of oviductal gestation
in amphibians. J. Exp. Zool. 266:394-413.
Wilbur, H. M. 1977. Propagule size, number, and dispersion pattern in Ambystoma and Asclepias.
Amer. Nat. 111:43-68.
Willham, R. L. 1963. The covariance between relatives for characters composed of components contributed by related individuals. Biometrics 19:18—
27.
Willham, R. L. 1972. The role of maternal effects in
animal breeding: III. Biometrical aspects of maternal effects in animals. J. Anim. Sci. 35:12881293.
Woodward, B. D. 1986. Paternal effects on juvenile
growth in Scaphiopus multiplicatus (the New
Mexico Spadefoot Toad). Amer. Nat. 128:58-65.
Woodward, B. D. 1987. Paternal effects on offspring
traits in Scaphiopus couchi (Anura: Pelobatidae).
Oecologia 73:626-629.
Wourms, J. P. and J. Lombardi. 1992. Reflections on
the evolution of piscine viviparity. Am. Zool. 32:
276-293.
Wourms, J. P., B. D. Grove, and J. Lombardi. 1988.
The maternal-embryonic relationship in vivparous
fishes. In W. S. Hoar and D. J. Randall (eds.), Fish
Physiology, Vol. X, Pt. b, pp. 1-134. Academic
Press, New York.
Zammuto, R. M. and J. S. Millar. 1985. Environmental predictability, variability, and Spermophilus
columbianus life history over an elevational gradient. Ecology 66:1784-1794.