Daphne J. Fairbairn

The evolution of trade-offs: where are we?

Trade‐offs are a core component of many evolutionary models, particularly those dealing with the evolution of life histories. In the present paper, we identify four topics of key importance for studies of the evolutionary biology of trade‐offs. First, we consider the underlying concept of ‘constraint’. We conclude that this term is typically used too vaguely and suggest that ‘constraint’ in the sense of a bias should be clearly distinguished from ‘constraint’ in the sense of proscribed combinations of traits or evolutionary trajectories. Secondly, we address the utility of the acquisition–allocation model (the ‘Y‐model’). We find that, whereas this model and its derivatives have provided new insights, a misunderstanding of the pivotal equation has led to incorrect predictions and faulty tests. Thirdly, we ask how trade‐offs are expected to evolve under directional selection. A quantitative genetic model predicts that, under weak or short‐term selection, the intercept will change but the slope will remain constant. Two empirical tests support this prediction but these are based on comparisons of geographic populations: more direct tests will come from artificial selection experiments. Finally, we discuss what maintains variation in trade‐offs noting that at present little attention has been given to this question. We distinguish between phenotypic and genetic variation and suggest that the latter is most in need of explanation. We suggest that four factors deserving investigation are mutation‐selection balance, antagonistic pleiotropy, correlational selection and spatio‐temporal variation, but as in the other areas of research on trade‐offs, empirical generalizations are impeded by lack of data. Although this lack is discouraging, we suggest that it provides a rich ground for further study and the integration of many disciplines, including the emerging field of genomics.

A COMPARATIVE ANALYSIS OF ALLOMETRY FOR SEXUAL SIZE DIMORPHISM: ASSESSING RENSCH'S RULE

Renschs rule states that sexual size dimorphism (SSD) increases with body size (hyperallometry) in taxa in which males are the larger sex and decreases with body size (hypoallometry) in those in which females are larger. We use the independent contrasts method to assess the validity and generality of Renschs rule within 21 independent animal taxa. Allometry is estimated as the slope of the major axis regression of contrasts for log(female size) versus contrasts for log(male size). Allometry consistent with Renschs rule is significant in 33% of the taxa examined across a diverse range of invertebrate and vertebrate taxa. Significant allometry inconsistent with Renschs rule occurs in only one taxon. Meta-analysis of these results reveals that Renschs rule is general and highly significant. Only owls have allometry inconsistent with this trend. Renschs rule is also shown to be associated with male-biased SSD, which is consistent with the hypothesis that sexual selection acting on male size drives the evolution of this pattern of allometry.

Sexual Selection and the Evolution of Allometry for Sexual Size Dimorphism in the Water Strider, Aquarius remigis

Sexual size dimorphism (SSD) typically increases with body size (hyperallometry) in taxa in which males are the larger sex and decreases with body size (hypoallometry) in taxa in which females are larger. We demonstrate the commonality of these trends, both of which indicate greater evolutionary divergence in male size than in female size and strong covariation between the sexes. We postulate that both of these components of allometry evolve in response to sexual selection on male size coupled with genetic correlations for size between males and females, and we argue that this hypothesis can be generalized to taxa in which females are the larger sex. For such taxa, we predict hypoallometry for SSD, sexual selection on male size, and a correlation between the intensity of sexual selection and male size. An analysis of total length in 31 populations of the water strider, Aquarius remigis, demonstrates significant hypoallometry for SSD. Comparisons of mating and single males within 12 populations reveal significant positive univariate or multivariate selection gradients in nine populations and a significant correlation between the intensity of sexual selection and mean male size, when environmentally based variation in mean size among sites is removed. These results provide the first quantitative evidence that allometry for SSD may evolve in response to sexual selection favoring large males, even in taxa in which females are the larger sex.

Proximate Causes of Rensch’s Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time?

A prominent interspecific pattern of sexual size dimorphism (SSD) is Rensch’s rule, according to which male body size is more variable or evolutionarily divergent than female body size. Assuming equal growth rates of males and females, SSD would be entirely mediated, and Rensch’s rule proximately caused, by sexual differences in development times, or sexual bimaturism (SBM), with the larger sex developing for a proportionately longer time. Only a subset of the seven arthropod groups investigated in this study exhibits Rensch’s rule. Furthermore, we found only a weak positive relationship between SSD and SBM overall, suggesting that growth rate differences between the sexes are more important than development time differences in proximately mediating SSD in a wide but by no means comprehensive range of arthropod taxa. Except when protandry is of selective advantage (as in many butterflies, Hymenoptera, and spiders), male development time was equal to (in water striders and beetles) or even longer than (in drosophilid and sepsid flies) that of females. Because all taxa show female‐biased SSD, this implies faster growth of females in general, a pattern markedly different from that of primates and birds (analyzed here for comparison). We discuss three potential explanations for this pattern based on life‐history trade‐offs and sexual selection.

Time and energy constraints and the evolution of sexual size dimorphism- to eat or to mate?

SummaryWe present an empirical test of the ‘Ghiselin—Reiss small-male hypothesis’ for the evolution of sexual size dimorphism (SSD). In mating systems dominated by scramble competition, where male reproductive success is a function of encounter rate with females, small males may be favoured when food is limiting because they require lower absolute amounts of food. Given a trade-off between time and energy devoted to foraging and to mate acquisition, small males should be able to devote more time to the latter. If at the same time larger females are favoured, this mechanism will contribute to the evolution of SSD and may be the major determinant of the female-biased SSDs that characterize most animal taxa. We tested this hypothesis using the water strider,Aquarius remigis (Heteroptera: Gerridae), a scramble competitor which mates many times over a prolonged mating season and which shows female-biased SSD. Laboratory experiments demonstrated that foraging success and giving up times (GUTs) are lower for males than for females during the reproductive season and that male water striders flexibly alter their time budgets under conditions of energy limitation. Controlled feeding experiments showed that male and female longevity, female fecundity and male mating success are positively related to food availability. As predicted, male body size is negatively correlated with several indices of male fitness (longevity, number of mating attempts and mating success), while female body size is positively correlated with longevity. These results are consistent with the hypothesis that scramble competition for mates favours small males in this species and provides empirical support for the Ghiselin—Reiss small-male hypothesis.

Factors Influencing Sexual Size Dimorphism in Temperate Waterstriders

Sexual size ratios (mean female length divided by mean male length) of 12 species of temperate waterstriders in the subfamily Gerrinae (Hemiptera, Gerridae) are analyzed to test both potentially nonadaptive and adaptive hypotheses for the evolution of sexual size dimorphism. Females tend to be larger than males, and regression of female length on male length (both log-transformed) reveals significant hypoallometry for size dimorphism. Both adaptive and nonadaptive explanations for the evolution of this allometry are discussed. Of these, only a nonadaptive model is consistent with the available data. Two closely related genera, Limnoporus and Gerris, are included in the data set, but covariance analysis reveals no significant effect of phylogeny on patterns of variation in size dimorphism. It is suggested, however, that the basic female bias may reflect descent from a common, highly dimorphic ancestor, rather than adaptation within this taxon. Four adaptive hypotheses are considered. Comparisons of the development times of males and females reveal that the female-biased size dimorphism is not associated with protandry, and the developmental-constraints hypothesis is therefore rejected. The hypothesis that selection for migration by flight tends to reduce sexual size dimorphism is supported by intraspecific comparisons of long-winged and short-winged morphs. A positive correlation between mating duration and residuals from the body-size regression supports the hypothesis that loading constraints associated with prolonged pairing select for increased size dimorphism. The available data on mating systems and size-selective mating support the hypothesis that sexual selection for large males promotes reduced or even reversed size dimorphism in some species, whereas sexual selection for large females increases size dimorphism in other species. Thus, patterns of size dimorphism in this taxon may be influenced by at least three, potentially interacting, selective processes: selection for dispersal by flight, selection for reduced loading during prolonged pairing, and sexual selection. The relative influence of these factors in three groups of ecologically similar species is discussed. The general conclusions of this study are consistent with the results of recent comparative studies of size dimorphism in primates. In both taxa, sexual size dimorphism is most strongly influenced by potentially nonadaptive factors, and the residual variation reflects the action of several selective factors. The complexity of size-ratio evolution revealed by these studies suggests that patterns of sizeratio variation within and among taxa, or size ratios typical of single species, are unlikely to be satisfactorily explained by reference to single hypotheses or to selective hypotheses only.

The Evolution and Genetics of Migration in Insects

ABSTRACT Because areas suitable for growth and reproduction are often ephemeral, a primary selective force in the evolution of migratory behavior in insects is the need to colonize new habitats. However, both migration itself and flight capability reduce present reproductive success. Thus the long-term fitness benefit of migration, the colonization of new habitats, is balanced by a short-term reduction in fitness, the result being that variation for migratory ability is preserved in a population. Migration is but one component of a wide suite of functionally connected traits that together form a migratory syndrome. Genetic variation is found in all components of the migratory syndrome, and selection for migration results in a change in the frequency of expression of these components, which can be analyzed and predicted using the mathematics of quantitative genetics. We illustrate this evolutionary interplay with the example of the evolution of wing dimorphism in the sand cricket.

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis.

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch’s rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch’s rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual‐selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential‐plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are “adaptively canalized.” While this hypothesis is unlikely to explain Rensch’s rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.

LIFETIME SELECTION ON ADULT BODY SIZE AND COMPONENTS OF BODY SIZE IN A WATERSTRIDER: OPPOSING SELECTION AND MAINTENANCE OF SEXUAL SIZE DIMORPHISM

Abstract.— Sexual size dimorphism (SSD), the difference in body size between males and females, is common in almost all taxa of animals and is generally assumed to be adaptive. Although sexual selection and fecundity selection alone have often been invoked to explain the evolution of SSD, more recent views indicate that the sexes must experience different lifetime selection pressures for SSD to evolve and be maintained. We estimated selection acting on male and female adult body size (total length) and components of body size in the waterstrider Aquarius remigis during three phases of life history. Opposing selection pressures for overall body size occurred in separate episodes of fitness for females in both years and for males in one year. Specific components of body size were often the targets of the selection on overall body size. When net adult fitness was estimated by combining each individuals fitnesses from all episodes, we found stabilizing selection in both sexes. In addition, the net optimum overall body size of males was smaller than that of females. However, even when components of body size had experienced opposing selection pressures in individual episodes, no components appeared to be under lifetime stabilizing selection. This is the first evidence that contemporary selection in a natural population acts to maintain female size larger than male size, the most common pattern of SSD in nature.

SEXUAL SIZE DIMORPHISM AS A CORRELATED RESPONSE TO SELECTION ON BODY SIZE: AN EMPIRICAL TEST OF THE QUANTITATIVE GENETIC MODEL

We artificially selected for body size in Drosophila melanogaster to test Landes quantitative genetic model for the evolution of sexual size dimorphism. Thorax width was used as an estimator of body size. Selection was maintained for 21 generations in both directions on males only, females only, or both sexes simultaneously. The correlated response of sexual size dimorphism in each selection regime was compared to the response predicted by four variants of the model, each of which differed only in assumptions about input parameters. Body size responded well to selection, but the correlated response of sexual size dimorphism was weaker than that predicted by any of the variants. Dimorphism decreased in most selection lines, contrary to the model predictions. We suggest that selection on body size acts primarily on growth trajectories. Changes in dimorphism are caused by the fact that male and female growth trajectories are not parallel and termination of growth at different points along the curves results in dimorphism levels that are difficult to predict without detailed knowledge of growth parameters. This may also explain many of the inconsistent results in dimorphism changes seen in earlier selection experiments.