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The Journal of Heredity 2002:93(6)
© 2002 The American Genetic Association 93:400-405

Maternal Effects and the Evolution of Behavioral and Morphological Characters: A Literature Review Indicates the Importance of Extended Maternal Care

K. Reinhold

From the Universität Bonn, Institut für Evolutionsbiologie und Ökologie, An der Immenburg 1, D-53121 Bonn, Germany.

Address correspondence to Klaus Reinhold at the address above, or e-mail: KReinhold{at}evolution.uni-bonn.de.


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Using literature data on reciprocal crosses, I estimated the influence of maternal effects on morphological and behavioral traits and compared these effects between mammals, birds, insects with homogametic females, and butterflies. In birds and in both groups of insects, no detectable difference between the reciprocal hybrids was observed on average, showing that in these groups, the contribution of maternal effects to the difference between the parental lines is at least rather small. In contrast to the other groups, mammals showed a significant and large influence of maternal effects on the examined characters. The large maternal effects in mammals are probably due to the extended period of parental care during gestation and lactation. It is concluded that maternal effects contributing to differences between parental lines are only widespread and important in mammals. It should be noted that these results do not show that maternal effects are absent in other animals. In the three examined groups, maternal effects may only evolve much more slowly than traits influenced by nuclear genes.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Phenotypic differences between individuals and the inheritance of these phenotypes are of fundamental importance to students of evolutionary biology because they are necessary prerequisites for phenotypic evolution. Since these two prerequisites are usually given, parents and offspring differ less from each other than unrelated individuals. A large part of this similarity is probably due to the sharing of nuclear genes, but inherited environmental effects (any influence of parents on offspring phenotype that is not caused by shared nuclear DNA) and effects of the cytoplasm might also contribute to the resemblance between parents and offspring. Recently it has been proposed that inherited environmental effects are of broad significance for phenotype evolution (Mousseau and Fox 1998; Wolf et al. 1998). In accordance with this hypothesis, one would expect that inherited environmental effects have a large and significant influence on many offspring traits.

Most of the inherited environmental effects on offspring phenotype are probably caused by the female producing the offspring. Due to the usual disparity in gamete size, females provide the majority of the zygote's cytoplasm and thus determine zygote size. Since the size or the content of the propagule might differ between females, these differences in maternal investment may influence offspring traits as a result. Moreover, it is usually the female that provides the offspring with care and nutrition. Under such a condition, offspring traits might become more similar to the mother's traits because of common environment or because learning or copying is involved. Here I define as maternal effects all those environmental effects that are inherited from the mother, such as cytoplasmic effects, and the effects of maternal investment or behavior on traits like offspring size or offspring behavior.

Maternal effects have been shown to be widespread and to influence a large variety of traits (Mousseau and Dingle 1991; Rossiter 1996). Among the diverse traits supposedly influenced by maternal effects are, for example, seed size in plants (Byers et al. 1997), diapause induction in insects (Mousseau and Dingle 1991), body size in lemmings (Boonstra and Hochachka 1997), lifespan in humans (Korpelainen 1999), and ovariole number in Drosophila (Starmer et al. 1998). Regarding many other traits, differences between reciprocal crosses are often attributed to maternal effects. However, there is neither an estimate on whether maternal effects are of general importance nor how large maternal effects are on average. Here I use literature data on reciprocal crosses to examine the relative contribution of maternal effects on phenotypic differences between subspecies, species, and races. I compare these estimates for the relative influence of maternal effects on behavioral and morphological traits between four groups of animals. In two of these four groups, maternal effects were examined for homogametic male offspring (birds and butterflies), and in the other two groups (mammals and insects with homogametic females) homogametic female offspring were examined. The analysis of the data shows that maternal effects are only widespread and significant in mammals.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Literature data on differences between reciprocal crosses were used to estimate the combined influence of maternal effects on quantitative morphological and behavioral characters. Appropriate data for the homogametic sex of insects, birds, and mammals were collected with an extensive literature search comprising more than 1000 articles. The combined influence of maternal effects was estimated from the difference in trait size between reciprocal crosses. To estimate the relative influence of these maternal effects I divided the difference between the two reciprocal hybrids by the difference between the two parental lines (see Equation 1).


where C is the character mean in the homogametic sex of parental strains A and B and their hybrids (the origin of the female is given first in the hybrid crosses).

The index ME calculated with Equation 1 enables us to compare the combined influence of all maternal effects on the different characters. An ME value of 0 shows no influence of maternal effects on the character under consideration. An ME value of 0.5 results when half of the phenotypic difference between the parental lines is caused by maternal effects. In such a case, both types of reciprocal hybrids of the homogametic sex resemble same-sex individuals from their mothers' line, but show only half the phenotypic difference of the parental lines. An ME value of 1 should occur when the difference between parental lines in the character under consideration is caused by only maternal effects. When there is no influence of maternal effects on a trait, some of the ME estimates should be positive and some negative because sampling or measurement error will generate differences in character size between reciprocal hybrids. It is therefore important not to use absolute values of ME estimates, because these absolute estimates would indicate maternal effects if there were large measurement errors but no maternal effects.

Data on parental lines with insignificantly different values were not used in the analysis presented here, because in these cases the calculated ME values are likely to be influenced mainly by chance. Likewise, those crosses where differences between parental lines were suggested to be due to single genes were not used. In a few cases, one of the hybrid crosses differed more from one parental line than two times the difference between the paternal lines. In these cases, the crosses were not used for the analysis because nonsymmetric hybrid dysgenesis or hybrid heterosis may erroneously lead to the notion of a large influence of maternal effects. In diallele crosses of more than two lines, several ME values can be calculated. To avoid using dependent data, only a single ME estimate was calculated, using the two parental lines that had the largest character difference within a given diallele cross. In some cases, several diallele crosses were given for the same trait within one article. In these cases I used only the average ME value for these crosses to avoid pseudo-replication. Also in order to avoid pseudo-replication, I averaged ME values when similar traits—that is, traits that supposedly measure the same or a genetically closely correlated character—were examined in the same genus in different publications. Those ME values that were averaged prior to any statistical analysis are indicated in Table 1 by the same lowercase letter in the trait column. The computed ME estimates for all available data points were compared between the following groups: butterflies, other insects with homogametic females, birds, and mammals.


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  		Table 1.. Estimated relative influence of maternal effects (see Methods for calculation of ME values) on diverse traits in homogametic female (insects and mammals) and homogametic male offspring (birds and butterflies).

 

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  		Table 1.. Table 1. Continued

 

   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
The average maternal effect did not significantly deviate from zero in butterflies (Wilcoxon one-sample test, Z = 0.36, n = 10, P >.5) and in other insects (Wilcoxon one-sample test, Z = 0.29, n = 26, P >.5). Even though no average effect was obvious, in a single study (Fox and Savalli 1998) a maternal effect explains all the difference in body size between two lines of a seed beetle (Table 1). On average, birds also showed a small and not significant influence of maternal effects on the examined traits (Wilcoxon one-sample test, Z = 0.04, n = 14, P >.5; see Figure 1). Only in mammals could a large and significant maternal effect be observed (Wilcoxon one-sample test, Z = 2.5, n = 23, P =.01). In this group, about one-quarter of the difference between the parental lines, on average, was caused by maternal effects (Figure 1). A comparison of the extent of maternal effects between groups shows a significant variation between groups ({chi}2 = 9.34, df = 3, P =.025). Post-hoc tests reveal that this variation is caused by a difference between mammals and the three other groups (pairwise Mann–Whitney U-tests, P <.05 for all comparisons with mammals and P >.05 for all comparisons between the three other groups). Within the mammals I compared the influence of maternal effects of growth- and size-related traits (those traits marked with bold genus names in Table 1) that are likely to be influenced by maternal investment with the maternal effects on those traits that are less obviously influenced by maternal provisioning. This comparison revealed a larger influence of maternal effects on growth- and size-related traits than on traits that were classified as being largely independent from maternal provisioning (Mann–Whitney U-test, n = 10,13, U = 22, P <.01).



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  		Figure 1.. Comparison of average maternal effects between the examined four different animal groups. The horizontal bars denote the arithmetic mean, the vertical bars denote the standard error, and the hatched line indicates the expected value when maternal effects are absent

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
On average, no significant maternal effect was observed in insects with homogametic and heterogametic females and in birds. The small average maternal effect should not be interpreted as evidence against the existence of maternal effects, since in one case, all the difference between the parental lines seems to be caused by maternal effects (Fox and Savalli 1998). In this specific case, maternal effects might allow an adaptive plastic response of seed beetles with respect to local population density. On average, however, large maternal effects seem to be rare, at least for the examined traits, and thus cannot serve as a general explanation for differences between parental lines. In contrast to the other groups, mammals showed a significant influence of maternal effects on the examined traits. Regarding the examined traits, maternal effects thus seem to be widespread and important in mammals.

How can we explain the observed difference between mammals and the other three groups? Female homogamy is unlikely to play a role, since the average maternal effect was very small in insects with homogametic females. Theoretically the maternal effects observed in mammals could also be due to mitochondrial effects. However, the large maternal effects on offspring size that were observed in mice and cattle were not related to mitochondrial effects (Dawson et al. 1993; Tess and MacNeil 1994). In mammals, the association between a female and her offspring is intense during gestation and lactation, and maternal care is often provided for an extended period. In line with this argument, offspring size and growth are often influenced by maternal age, size, and condition (e.g., Ellis et al. 2000). According to this hypothesis, those traits that are especially likely to be influenced by maternal care—growth, maturation, body size—should show larger maternal effects than other traits. In accordance with this hypothesis, maternal effects for these traits are larger than maternal effects for traits that are less likely to be influenced by maternal care. Nine of 10 size- and growth-related traits have ME values greater than 0.2, whereas 12 of 13 other traits have ME values less than 0.2. The one clear exception is nesting behavior in mice (Lee 1973), which has an ME value of about 1. In this case, offspring learning might have been involved. Among the remaining 12 traits not obviously related to size and growth, the mean (0.02) is very close and not significantly different from zero (Wilcoxon one-sample test, Z = 0.55, n = 12, P >.5). Thus it seems likely that maternal effects in mammals are caused by and largely limited to effects of maternal offspring provisioning.

Offspring provisioning with food might be expected to lead to large maternal effects in songbirds (Potti 1999). This expectation does not contradict the results of the present study, since ME values on altricial birds are not available and because all the data given in Table 1 are from precocial birds. However, maternal effects independent from offspring feeding can, for example, be achieved by differential egg provisioning (Gil et al. 1999; Royle et al. 2001). Maternal behavior may also cause maternal effects without provisioning of offspring: in a lizard, maternal basking was recently shown to have a large influence on offspring phenotype and growth (Wapstra 2000).

In accordance with the argument that maternal provisioning is the source for maternal effects in mammals, maternal effects should diminish later in offspring life. A decreasing influence of maternal effects with offspring age is observed in most cases (Cundiff 1972; Legates 1972; but see Gregory and Maurer 1991). Such a decrease in the impact of maternal effects with offspring age is not limited to mammals. Similar effects have also been shown to occur in fish, where fry size but not adult size of offspring is largely determined by maternal effects (Heath et al. 1999).

For some traits, such as body weight in mice, the available ME values differ to a large extent so that in the chosen example, six values ranging from 0.1 to 1.1 were estimated. An effect of age on the estimated maternal effects, as discussed in the last paragraph, is unlikely to explain this large variation between ME estimates. The two studies that resulted in relatively large ME estimates (Schüler and Borodin 1976, 1978) measured body weight when mice were youngest (6 weeks) and oldest (18–19 weeks) compared with the other studies used to estimate ME values for body size in mice. Since no obvious differences between these two studies and the others, for example, with respect to inbreeding status, body weight, and differences in body weight between parental lines, can explain the received variation in ME values, animal breeding conditions might have a large influence on the extent of maternal effects on body size in mice.

The absence of large maternal effects in the two insect groups fits the fact that maternal effects have been found to have no influence on, for example, mating behavior in Drosophila mojavensis (Zouros 1981), eyestalk length in stalk-eyed flies (Wolfenbarger and Wilkinson 2001), and insecticide resistance in moth larvae (Thomas and Boethel 1995). However, significant maternal effects have been found for ethanol tolerance in Drosophila (Kerver and Rotman 1987), and facultative egg diapause often seems to be controlled by maternal effects in insects (e.g., Hockham et al. 2001). In insects, maternal effects thus seem to be rare, but whenever they occur they can have a large influence on offspring traits. However, in all cases where maternal effects were large in insects and birds (Fox and Savalli 1998; Gil et al. 1999; Hockham et al. 2001; Kerver and Rotman 1987; Royle et al. 2001), the observed maternal effects are closely related to phenotype plasticity and seem to serve a function analogous to a phenotype-genotype interaction.

From the reviewed literature it is concluded that maternal effects contributing to differences between parental lines are only widespread and important in mammals. It should be noted that the presented results do not show that maternal effects are absent in other animals. In the three nonmammalian groups examined here, maternal effects may only evolve much slower than traits influenced by nuclear genes. Under such a scenario, crosses between selected lines, subspecies, or closely related species that will only reveal the accumulated differences are unlikely to show much evidence of maternal effects.


   Acknowledgments
 
I am grateful to the Institute for Advanced Study in Berlin for supporting the initial data collection, and I thank Leif Engqvist for his helpful comments on the manuscript.


   Footnotes
 
Corresponding Editor: Stephen J. O'Brien Back

Received April 2, 2002
Accepted September 30, 2002


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