A search for trade-offs among life history traits inDrosophila melanogaster

Summary Are there underlying developmental and physiological properties of organisms that can be used to build a general theory of life history evolution? Much of the theoretical work on the evolution of life histories is based on the premise of negative developmental and genetic correlations among life history traits. If negative correlations do not exist as a general rule then no general theory taking them into account is possible. Negative genetic correlations among life history traits can come about by antagonistic pleiotropy. One cause of antagonistic pleiotropy is cost allocation trade-offs. Since cost allocation trade-offs are due to underlying physiological constraints they are expected to be common to closely related groups. A second form of antagonistic pleiotropy is specialization of genotypes to different niches. This type of antagonistic pleiotropy is expected to be specific to each population. We looked for trade-offs in life history traits of longevity and fecundity inDrosophila melanogaster. We used a half-sib mating design and raised the offspring at two temperatures, 19°C and 25°C. Correlations between longevity and fecundity showed some evidence of antagonistic pleiotropy at high temperature with no evidence of any trade-offs at low temperature. Correlations of early and late fecundity traits did show evidence of cost allocation trade-offs at both temperatures. Antagonistic pleiotropy was also found for cross-environmental correlations of fecundity traits. We conclude that, although life history trade-offs can not be generally assumed, they are frequently found among functionally related traits. Thus, we provide guidelines for the development of general theories of life history evolution.     

The importance of growth and mortality costs in the evolution of the optimal life history

A central assumption of life history theory is that the evolution of the component traits is determined in part by trade-offs between these traits. Whereas the existence of such trade-offs has been well demonstrated, the relative importance of these remains unclear. In this paper we use optimality theory to test the hypothesis that the trade-off between present and future fecundity induced by the costs of continued growth is a sufficient explanation for the optimal age at first reproduction, alpha, and the optimal allocation to reproduction, G, in 38 populations of perch and Arctic char. This hypothesis is rejected for both traits and we conclude that this trade-off, by itself, is an insufficient explanation for the observed values of alpha and G. Similarly, a fitness function that assumes a mortality cost to reproduction but no growth cost cannot account for the observed values of alpha. In contrast, under the assumption that fitness is maximized, the observed life histories can be accounted for by the joint action of trade-offs between growth and reproductive allocation and between mortality and reproductive allocation (Individual Juvenile Mortality model). Although the ability of the growth/mortality model to fit the data does not prove that this is the mechanism driving the evolution of the optimal age at first reproduction and allocation to reproduction, the fit does demonstrate that the hypothesis is consistent with the data and hence cannot at this time be rejected. We also examine two simpler versions of this model, one in which adult mortality is a constant proportion of juvenile mortality [Proportional Juvenile Mortality (PJM) model] and one in which the proportionality is constant within but not necessarily between species [Specific Juvenile Mortality (SSJM) model]. We find that the PJM model is unacceptable but that the SSJM model produces fits suggesting that, within the two species studied, juvenile mortality is proportional to adult mortality but the value differs between the two species.     

Correlated evolution between male ejaculate allocation and female remating behaviour in seed beetles (Bruchidae)

Sperm competition theory suggests that female remating rate determines the selective regime that dictates the evolution of male ejaculate allocation. To test for correlated evolution between female remating behaviour and male ejaculate traits, we subjected detailed experimental data on female and male reproductive traits in seven-seed beetle species to phylogenetic comparative analyses. The evolution of a larger first ejaculate was positively correlated with the evolution of a more rapid decline in ejaculate size over successive matings. Further, as predicted by theory, an increase in female remating rate correlated with the evolution of larger male testes but smaller ejaculates. However, an increase in female remating was associated with the evolution of a less even allocation of ejaculate resources over successive matings, contrary to classic sperm competition theory. We failed to find any evidence for coevolution between the pattern of male ejaculate allocation and variation in female quality and we conclude that some patterns of correlated evolution are congruent with current theory, whereas some are not. We suggest that this may reflect the fact that much sperm competition theory does not fully incorporate other factors that may affect the evolution of male and female traits, such as trade-offs between ejaculate expenditure and other competing demands and the evolution of resource acquisition.     

When relative allocation depends on total resource acquisition: implication for the analysis of trade‐offs

A central tenet of evolutionary biology states that life‐history traits are linked via trade‐offs, as classically exemplified by the van Noordwijk and de Jong model. This model, however, assumes that the relative resource allocation to a biological function varies independently of the total resource acquisition. Based on current empirical evidence, we first explored the dependency between the total resource acquisition and the relative resource allocation to reproduction and showed that such dependency is the rule rather than the exception. We then derived the expression of the covariance between traits when the assumption of independence is relaxed and used simulations to quantify the importance of such dependency on the detection of trade‐offs between current reproduction and future survival. We found that the dependency between the total energy acquisition and the relative allocation to reproduction can influence the probability to detect trade‐offs between survival and reproduction. As a general rule, a negative dependency between the total energy acquisition and the relative allocation to reproduction should lead to a higher probability of detecting a trade‐off in species with a fast pace of life, whereas a positive dependency should lead to a higher probability of detecting a trade‐off in species with a slow pace of life. In addition to confirming the importance of resource variation to reveal trade‐offs, our finding demonstrates that the covariance between resource allocation and resource acquisition is generally not null and also plays a fundamental role in the detection of trade‐offs.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Offspring size-number trade-offs in scorpions: an empirical test of the van Noordwijk and de Jong model

Abstract Life-history traits are expected to exhibit negative phenotypic trade-offs, but often do not. In a seminal paper, van Noordwijk and de Jong (1986) provided an answer to this seeming paradox. According to their model, trade-offs will be more difficult to detect if variation in resource acquisition (or investment) is high relative to variation in resource allocation to the traits under consideration. Despite its influence on subsequent life-history studies, this model has rarely been tested. I use data from 10 species of scorpion (a total of 30 datasets, including multiple populations or years for some species) to test the van Noordwijk-de Jong model as modified to examine the relationship between offspring size and number. For both the overall data and a subset, including only the species Centruroides vittatus , I found that the correlation between offspring size and number within a population was significantly negatively correlated with the ratio of allocation variance to investment variance. That is, strong trade-offs were found when the investment variance was low relative to the allocation variance. These results were robust to the particular measure of offspring size and to whether offspring data were adjusted for female size variation. My results therefore provide strong evidence in support of the van Noordwijk and de Jong model.     

The evolutionary genetics of acquisition and allocation in the wing dimorphic cricket, Gryllus firmus

The evolutionary trajectories of trade-offs are ultimately governed by the evolution of the underlying physiological processes of the acquisition and subsequent allocation of resources. In this study, we focused directly on acquisition and allocation as traits and estimated their genetic architecture in the trade-off between flight capability and reproduction in the cricket, Gryllus firmus. To determine the evolutionary genetics of acquisition and allocation both within and between resource environments, we performed a large-scale quantitative genetic breeding experiment in which families were split over several resource levels. Our findings were fourfold: (1) there was substantial genetic variance in acquisition and allocation, (2) contrary to the assumption of independence between acquisition and allocation, there was a significant genetic correlation between them, (3) the genetic covariance between acquisition and allocation was significantly different in the different food environments, (4) the trade-off, as measured by the genetic correlation between flight muscle mass and ovary mass, was only significant in the food restriction environments. However, when measured directly as the genetic correlation between reproductive allocation and flight allocation, we found a consistent strong negative genetic correlation, demonstrating that when allocation is measured independently of acquisition we find evidence for the trade-off.     

Positive genetic correlations among major life-history traits related to ecological success in the aphid Myzus persicae

Life-history theory is based on the assumption that evolution is constrained by trade-offs among different traits that contribute to fitness. Such trade-offs should be evident from negative genetic correlations among major life-history traits. However, this expectation is not always met. Here I report the results of a life-table experiment designed to measure the broad-sense heritabilities of life-history traits and their genetic correlations in 19 different clones of the aphid Myzus persicae from Victoria, Australia. Most individual traits, as well as fitness calculated as the finite rate of increase from the life table, exhibited highly significant heritabilities. The pattern of genetic correlations revealed absolutely no evidence for life-history trade-offs. Rather, life histories were arranged along an axis from better to worse. Clones with shorter development times tended to have larger body sizes, higher fecundities, and larger offspring. The fitness of clones estimated from the life table in the laboratory tended to be positively associated with their abundance in the field. Fitness also increased significantly with heterozygosity at the seven microsatellite loci that were used to distinguish clones and estimate their frequencies in the field. I discuss these findings in light of a recent proposition that positive genetic correlations among life-history traits for which trade-offs are expected can be explained by genetic variation for resource acquisition ability that is maintained in populations by a cost of acquisition, and I propose ways to test for such a cost in M. persicae.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

Phenotypic plasticity of life history traits in relation to reproductive strategies in <Emphasis Type="Italic">Boa constrictor occidentalis</Emphasis>

The close connection between reproductive ecology and life history in snakes leads to trade-offs between reproductive and other life-history traits. Optimal energy allocation to growth and reproduction is a key factor to determine life history structure. Therefore, elucidating the relationship between body size variations and reproductive characters is essential for a better understanding of life-history plasticity. The aim of this work was to determine to what extent life-history differs among populations of Boa constrictor occidentalis and to identify possible life-history trade-offs between morphological and reproductive traits. We compared two populations from areas that are separated latitudinally, with different climatic conditions and vegetation landscape structure. Reproductive and morphological data of specimens were recorded. Although populations had a similar mean length of mature snakes, the frequency of some size classes tended to be different. Size at sexual maturity differed between populations for females, generating variations in the proportion of mature individuals. Reproductive threshold and follicular size also varied, but female reproductive frequency was similar between populations. Reproductive frequency of males varied between populations although their body condition was similar. We discussed two major issues: (1) implications of size at sexual maturity for body size and fecundity; (2) trade-offs in reproductive characters.     

Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all?

On the basis of physiological and ecological costs of defense allocation, most plant defense theories predict the occurrence of trade-offs between resource investment in different types of antiherbivore defenses. To test this prediction, we conducted a meta-analysis of 31 studies published in 1976-2002 that provided data on covariation of different defensive traits in plant genotypes. We found no overall negative association between different defensive traits in plants; instead, the relationship between defensive traits varied from positive to negative depending on the types of co-occurring defenses. Evidence of trade-off was found only between constitutive and induced defenses. Therefore, to a large extent, plants appear to be jacks-of-all-trades, masters of all and may successfully produce several types of defense without paying considerable trade-offs. Our survey thus provides little evidence that genetic trade-offs between defensive traits significantly constrain the evolution of multiple defenses in plants.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

Trade-offs between sexual and clonal reproduction in an aquatic plant: experimental manipulations vs. phenotypic correlations

That trade-offs result from the allocation of limited resources is a central concept of life history evolution. We quantified trade-offs between sexual and clonal reproduction in the aquatic plant, Butomus umbellatus, by experimentally manipulating sexual investment in two distinct nutrient environments. Increasing seed production caused a significant but nonlinear trade-off. Pollinating half of all flowers strongly reduced clonal bulbil production, but pollinating the remaining flowers did not cause any further trade-off. Trade-offs were not stronger under low nutrient conditions that clearly limited plant growth. Experimentally induced trade-offs were not reflected in negative phenotypic correlations between sexual and clonal allocation among plants within eight populations grown in a uniform greenhouse environment. Diminishing effects of increased sexual allocation plus a lack of accord between experimental manipulations and phenotypic correlations suggest that trade-offs between sexual and clonal reproduction are unlikely to constrain the evolution of reproductive strategy in this species.     

Analytic and simulation models predicting positive genetic correlations between traits linked by trade-offs

Summary Using a two-loci multiplicative model of resource allocation, we show how the existence of several levels of resource allocation may affect the sign of the genetic correlations between traits linked by trade-offs. Positive genetic correlations between components of fitness affected by genetic trade-offs may result from different amounts of genetic variability at the pleiotropic loci determining the allocation of resources. Thus positive genetic correlations may be obtained in the absence both of environmental variation and of differences between individuals in resource acquisition. Nevertheless, positive correlations between all components of fitness at the same time cannot be obtained without variability in the acquisition of resources.     

A critique of methods for measuring life history trade-offs

Constraints have important effects on the evolution of life history strategies, but several difficulties have been encountered in determining constraints empirically. Here we investigate methods for measuring a specific type of constraint known as a trade-off. A trade-off between two traits implies a perfect negative correlation between the traits. Trade-offs may involve more than two traits, however, and pairs of traits involved in such a higher-dimensional trade-off may be positively correlated. If some of the traits involved in a trade-off are omitted from the experimental design, the trade-off may not even be detectable. Direct measures of trade-offs are thus complicated, and indirect means of identifying trade-offs may often provide the only feasible measures.     

The evolutionary convergence of avian lifestyles and their constrained coevolution with species' ecological niche

The fit between life histories and ecological niche is a paradigm of phenotypic evolution, also widely used to explain patterns of species co-occurrence. By analysing the lifestyles of a sympatric avian assemblage, we show that species'' solutions to environmental problems are not unbound. We identify a life-history continuum structured on the cost of reproduction along a temperature gradient, as well as habitat-driven parental behaviour. However, environmental fit and trait convergence are limited by niche filling and by within-species variability of niche traits, which is greater than variability of life histories. Phylogeny, allometry and trade-offs are other important constraints: lifetime reproductive investment is tightly bound to body size, and the optimal allocation to reproduction for a given size is not established by niche characteristics but by trade-offs with survival. Life histories thus keep pace with habitat and climate, but under the limitations imposed by metabolism, trade-offs among traits and species'' realized niche.     

Macroclimatic and maternal effects on the evolution of reproductive traits in lizards

Much of life‐history theory rests on fundamental assumptions about constraints on the acquisition and allocation of energy to growth and reproduction. In general, the allocation of energy to reproduction depends on maternal size, which in turn depends on environmental factors experienced throughout the life of the mother. Here, we used phylogenetic path analyses to evaluate competing hypotheses about the environmental and maternal drivers of reproductive traits in lizards. In doing so, we discovered that precipitation, rather than temperature, has shaped the evolution of the life history. Specifically, environments with greater rainfall have enabled the evolution of larger maternal size. In turn, these larger mothers produce larger clutches of larger offspring. However, annual precipitation has a negative direct effect on offspring size, despite the positive indirect effect mediated by maternal size. Possibly, the evolution of offspring size was driven by the need to conserve water in dry environments, because small organisms are particularly sensitive to water loss. Since we found that body size variation among lizards is related to a combination of climatic factors, mainly precipitation and perhaps primary production, our study challenges previous generalizations (e.g., temperature‐size rule and Bergmann''s rule) and suggests alternative mechanisms underlying the evolution of body size.     

The Rate-Size Trade-Off Structures Intraspecific Variation in Daphnia ambigua Life History Parameters

The identification of trade-offs is necessary for understanding the evolution and maintenance of diversity. Here we employ the supply-demand (SD) body size optimization model to predict a trade-off between asymptotic body size and growth rate. We use the SD model to quantitatively predict the slope of the relationship between asymptotic body size and growth rate under high and low food regimes and then test the predictions against observations for Daphnia ambigua. Close quantitative agreement between observed and predicted slopes at both food levels lends support to the model and confirms that a ‘rate-size’ trade-off structures life history variation in this population. In contrast to classic life history expectations, growth and reproduction were positively correlated after controlling for the rate-size trade-off. We included 12 Daphnia clones in our study, but clone identity explained only some of the variation in life history traits. We also tested the hypothesis that growth rate would be positively related to intergenic spacer length (i.e. the growth rate hypothesis) across clones, but we found that clones with intermediate intergenic spacer lengths had larger asymptotic sizes and slower growth rates. Our results strongly support a resource-based optimization of body size following the SD model. Furthermore, because some resource allocation decisions necessarily precede others, understanding interdependent life history traits may require a more nested approach.     

The genetics of primary and secondary sexual character trade-offs in a horned beetle

When structures compete for shared resources, this may lead to acquisition and allocation trade-offs so that the enlargement of one structure occurs at the expense of another. Among the studies of morphological trade-offs, their importance has been demonstrated primarily through experimental manipulations and comparative analyses. Relatively, a few studies have investigated the underlying genetic basis of phenotypic patterns. Here, we use a half-sibling breeding design to determine the genetic underpinnings of the phenotypic trade-off between head horns and the male copulatory organ or aedeagus that has been found in the dung beetle Onthophagus taurus. Instead of the predicted negative genetic covariance among characters that trade-off, we find positive genetic covariance between absolute horn and aedeagus length and zero genetic covariance between relative horn and aedeagus length. Therefore, although the genetic covariance between absolute horn and aedeagus length would constrain the independent evolution of primary and secondary sexual characters in this population, there was no evidence of a trade-off. We discuss alternative hypotheses for the observed patterns of genetic correlation between traits that compete for resources and the implications that these have for selection and the evolution of such traits.     

Size-dependent predation and correlated life history traits alter eco-evolutionary dynamics and selection for faster individual growth

Age at maturation is a key life history trait influencing individual fitness, population age structure, and ecological interactions. We investigated the evolution of age at maturity through changes in the von Bertalanffy growth constant for organisms with a simple juvenile-adult life history. We used Gillespie eco-evolutionary models to uncover the role of predation in driving the evolution of the growth constant when eco-evolutionary dynamics are present. We incorporated both size-independent and size-dependent predation into our models to generate differences in selection and dynamics in the system. Our results generally support the idea that faster ontogenetic growth is beneficial when populations are growing but that predation tends to have little effect on age at maturity unless there are trade-offs with other life history traits. In particular, if faster ontogenetic growth comes at the cost of fecundity, our results suggest that predation selects for intermediate levels of growth and fecundity. Eco-evolutionary dynamics influenced the nature of selection only when growth was linked to fecundity. We also found that predators that increasingly consume larger prey tend to have higher population sizes due to the greater energy intake from larger prey, but the growth rate-fecundity trade-off reversed this pattern. Overall, our results suggest an important role for interactions between size-dependent foraging and life-history trade-offs in generating varying selection on age at maturity through underlying growth traits.