Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.     

DOES THE TRADE-OFF BETWEEN GROWTH AND REPRODUCTION SELECT FOR FEMALE-BIASED SEXUAL ALLOCATION IN COSEXUAL PLANTS?

We analyzed sexual allocation in cosexual plants while taking the trade-off between growth and reproduction into consideration and showed that this trade-off does not select for female-biased sexual allocation. There are two problems in sexual allocation: optimizing the amount of resources allocated to reproduction in a growing season and equalizing the resources allocated to the male and the female functions. If these two are possible at the same time, equal resource allocation to the male and the female functions is the evolutionarily stable strategy (ESS; given that the fitness gains through the male and the female functions are proportional to the amount of the resources allocated to these functions). Biased sexual allocation only occurs when constraints make it impossible to simultaneously optimize allocation to reproduction and allocation to male and female functions. However, even if female-biased sexual allocation occurs due to the addition of other constraints, the trade-off between growth and reproduction itself is not an important factor that selects for female-biased sexual allocation.     

Sex allocation in a simultaneously hermaphroditic marine shrimp

Two fundamental questions dealing with simultaneous hermaphrodites are how resources are optimally allocated to the male and female function and what conditions determine shifts in optimal sex allocation with age or size. In this study, I explored multiple factors that theoretically affect fitness gain curves (that depict the relationship between sex-specific investment and fitness gains) to predict and test the overall and size-dependent sex allocation in a simultaneously hermaphroditic brooding shrimp with an early male phase. In Lysmata wurdemanni, sperm competition is absent as hermaphrodites reproducing in the female role invariably mated only once with a single other shrimp. Shrimps acting as females preferred small over large shrimps as male mating partners, male mating ability was greater for small compared to large hermaphrodites, and adolescent males were predominant in the population during the breeding season. In addition, brooding constraints were not severe and varied linearly with body size whereas the ability to acquire resources increased markedly with body size. Using sex allocation theory as a framework, the findings above permitted to infer the shape of the male and female fitness gain curves for the hermaphrodites. The absence of sperm competition and the almost unconstrained brooding capacity imply that both curves saturate, however the male curve levels off much more quickly than the female curve with increasing level of investment. In turn, the predominance of adolescent males in the population implies that the absolute gain of the female curve is greater than that of the male curve. Last, the size-dependent female preference and male mating ability of hermaphrodites determines that the absolute gain of the male curve is greater for small than for large hermaphrodites. Taking into consideration the inferred shape of the fitness gain curves, two predictions with respect to the optimal sex allocation were formulated. First, overall sex allocation should be female biased; it permits hermaphrodites to profit from the female function that provides a greater fitness return than the male function. Second, sex allocation should be size-dependent with smaller hermaphrodites allocating more than proportionally resources to male reproduction than larger ones. This size-dependent sex allocation permits hermaphrodites to profit from male mating opportunities that are the greatest at small body sizes. Size-dependent sex allocation is also expected because the male fitness gain curve decelerates more quickly than the female gain curve and experiments indicated that resources are greater for large than small hermaphrodites. These two predictions were tested when determining the sex allocation of hermaphrodites by dissecting their gonad and quantifying ovaries versus testes mass. Supporting the predictions above, hermaphrodites allocated, on average, 118 times more to the female than to the male gonad and the proportion of resources devoted to male function was higher in small than in large hermaphrodites. A trade-off between male and female allocation is assumed by theory but no negative correlation between male and female reproductive investment was observed. In L. wurdemanni, the relationship between sex-specific investment and fitness changes during ontogeny in a way that is consistent with an adjustment of sex allocation to improve size-specific reproductive success.     

Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp

Sex allocation theory for simultaneous hermaphrodites assumes a direct trade-off between the allocation of resources to the male and female reproductive functions. Empirical support for this basic assumption is scarce, possibly because studies rarely control for variation in individual reproductive resource budgets. Such variation, which can have environmental or genetic sources, can generate a positive relationship between male and female investment and can thus obscure the trade-off. In this study on the hermaphroditic flatworm Macrostomum sp. we tried to control for budget effects by restricting food availability in a standardized way and by using an inbred line. We then manipulated mating group size in a two-way design (two group sizes x two enclosure sizes) in order to induce phenotypic variation in male allocation, and expected to find an opposing correlated response in female allocation. The results suggest that we only managed to control the budget effects under some conditions. Under these the sex allocation trade-off emerged. Under the other conditions we found a strongly positive correlation between male and female allocation. We discuss possible causes for the observed differences.     

The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

First principles of thermodynamics imply that metabolic pathways are faced with a trade-off between the rate and yield of ATP production. Simple evolutionary models argue that this trade-off generates a fundamental social conflict in microbial populations: average fitness in a population is highest if all individuals exploit common resources efficiently, but individual reproductive rate is maximized by consuming common resources at the highest possible rate, a scenario known as the tragedy of the commons. In this paper, I review studies that have addressed two key questions: What is the evidence that the rate-yield trade-off is an evolutionary constraint on metabolic pathways? And, if so, what determines evolutionary outcome of the conflicts generated by this trade-off? Comparative studies and microbial experiments provide evidence that the rate-yield trade-off is an evolutionary constraint that is driven by thermodynamic constraints that are common to all metabolic pathways and pathway-specific constraints that reflect the evolutionary history of populations. Microbial selection experiments show that the evolutionary consequences of this trade-off depend on both kin selection and biochemical constraints. In well-mixed populations with low relatedness, genotypes with rapid and efficient metabolism can coexist as a result of negative frequency-dependent selection generated by density-dependent biochemical costs of rapid metabolism. Kin selection can promote the maintenance of efficient metabolism in structured populations with high relatedness by ensuring that genotypes with efficient metabolic pathways gain an indirect fitness benefit from their competitive restraint. I conclude by suggesting avenues for future research and by discussing the broader implications of this work for microbial social evolution.     

The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

First principles of thermodynamics imply that metabolic pathways are faced with a trade-off between the rate and yield of ATP production. Simple evolutionary models argue that this trade-off generates a fundamental social conflict in microbial populations: average fitness in a population is highest if all individuals exploit common resources efficiently, but individual reproductive rate is maximized by consuming common resources at the highest possible rate, a scenario known as the tragedy of the commons. In this paper, I review studies that have addressed two key questions: What is the evidence that the rate-yield trade-off is an evolutionary constraint on metabolic pathways? And, if so, what determines evolutionary outcome of the conflicts generated by this trade-off? Comparative studies and microbial experiments provide evidence that the rate-yield trade-off is an evolutionary constraint that is driven by thermodynamic constraints that are common to all metabolic pathways and pathway-specific constraints that reflect the evolutionary history of populations. Microbial selection experiments show that the evolutionary consequences of this trade-off depend on both kin selection and biochemical constraints. In well-mixed populations with low relatedness, genotypes with rapid and efficient metabolism can coexist as a result of negative frequency-dependent selection generated by density-dependent biochemical costs of rapid metabolism. Kin selection can promote the maintenance of efficient metabolism in structured populations with high relatedness by ensuring that genotypes with efficient metabolic pathways gain an indirect fitness benefit from their competitive restraint. I conclude by suggesting avenues for future research and by discussing the broader implications of this work for microbial social evolution.     

Extracting the underlying physiological determinants of resource-based trade-offs: a principal components approach

Abstract The relationship between traits that compete for resources is influenced by variance in the acquisition and allocation of resources. The difficulty of accurately measuring these underlying physiological processes has hampered studies of resource-based trade-offs. Here, we explore the ability of principal components analysis (PCA) to extract axes corresponding to acquisition and allocation in a bivariate trade-off by comparing these axes to estimates obtained using physiological measurements. We validate the method using simulations and then test it using empirical data for the well-characterized trade-off between flight capability and reproduction in female sand crickets, Gryllus firmus. We find a high correspondence between our physiological estimates and the estimates obtained using PCA. Our results demonstrate that PCA provides a robust and efficient method for estimating acquisition and allocation directly from the traits involved in a resource-based trade-off.     

5种毛茛科植物个体大小依赖的繁殖分配和性分配

 植物繁殖分配和性分配是生活史理论的核心问题,一直受到生态学家、进化生物学家们的关注。通过对青藏高原东部高寒草甸(3 500 m)及亚高山草甸(2 900 m)毛茛科5种虫媒两性花植物花期的繁殖分配和性分配的研究发现：1）个体越大,繁殖投入越高,繁殖分配越低,与以往研究结果一致;2）性分配是个体大小依赖的,大个体更偏向雌性器官的资源投入,花粉胚珠比与个体大小的关系较复杂,因种而异;3）花期雌雄功能之间存在资源分配上的权衡（Trade-off）,并且种群之间有差异,表明其受环境条件影响。     

青藏高原高寒草甸植物花寿命与花吸引特征的关系及其对雌性繁殖成功的影响

花寿命指花保持开放且具有功能的时间长度, 是开花植物繁殖成功的一个重要功能性状。可塑性延长花寿命是植物在不利的传粉环境中保障繁殖的一种策略, 但延长花寿命也会增加繁殖成本。花寿命的可塑性变异不仅受传粉环境的影响, 而且还受资源分配权衡的影响。花寿命的理论模型指出, 植物的花寿命与花吸引特征之间存在资源分配权衡。为了研究在花粉限制环境中, 植物花寿命与花吸引特征之间的资源权衡及其对雌性适合度的相对重要性。该研究以青藏高原高寒草甸不同海拔(2 900和3 600 m)的11种开花植物为研究对象, 分析了不同植物群落中, 物种水平上: (1)花寿命与花吸引特征(花大小以及开花数目)之间的相关关系; (2)花寿命与花吸引特征对植物雌性适合度的相对贡献。结果表明, 无论是低海拔还是高海拔植物群落, 植物的花寿命与开花数目之间均存在权衡关系, 且长的花寿命增加了植物的雌性适合度。但在高海拔环境中, 植物的雌性适合度只与花寿命有关。这说明相对于低海拔植物, 花寿命对高海拔植物的雌性繁殖成功更为重要。     

Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect

Optimisation of reproductive investment is crucial for Darwinian fitness, and detailed long-term studies are especially suited to unravel reproductive allocation strategies. Allocation strategies depend on the timing of resource acquisition, the timing of resource allocation, and trade-offs between different life-history traits. A distinction can be made between capital breeders that fuel reproduction with stored resources and income breeders that use recently acquired resources. In capital breeders, but not in income breeders, energy allocation may be decoupled from energy acquisition. Here, we tested the influence of extrinsic (weather conditions) and intrinsic (female characteristics) factors during energy storage, vitellogenesis and early gestation on reproductive investment, including litter mass, litter size, offspring mass and the litter size and offspring mass trade-off. We used data from a long-term study of the viviparous lizard, Lacerta (Zootoca) vivipara. In terms of extrinsic factors, rainfall during vitellogenesis was positively correlated with litter size and mass, but temperature did not affect reproductive investment. With respect to intrinsic factors, litter size and mass were positively correlated with current body size and postpartum body condition of the previous year, but negatively with parturition date of the previous year. Offspring mass was negatively correlated with litter size, and the strength of this trade-off decreased with the degree of individual variation in resource acquisition, which confirms theoretical predictions. The combined effects of past intrinsic factors and current weather conditions suggest that common lizards combine both recently acquired and stored resources to fuel reproduction. The effect of past energy store points out a trade-off between current and future reproduction.     

Environmental uncertainty, autocorrelation and the evolution of survival

Survival is a key fitness component and the evolution of age- and stage-specific patterns in survival is a central question in evolutionary biology. In variable environments, favouring chances of survival at the expense of other fitness components could increase fitness by spreading risk across uncertain conditions, especially if environmental conditions improve in the future. Both the magnitude of environmental variation and temporal autocorrelation in the environment might therefore affect the evolution of survival patterns. Despite this, the influence of temporal autocorrelation on the evolution of survival patterns has not been addressed. Here, we use a trade-off structure which reflects the empirically inspired paradigm of acquisition and allocation of resources to investigate how the evolutionarily stable survival probability is shaped in variable, density-dependent environments. We show that temporal autocorrelation is likely to be an important aspect of environmental variability that contributes to shaping age- and stage-specific patterns of survival probabilities in nature.     

Physiological dynamics,reproduction‐maintenance allocations,and life history evolution

Allocation of resources to competing processes of growth, maintenance, or reproduction is arguably a key process driving the physiology of life history trade‐offs and has been shown to affect immune defenses, the evolution of aging, and the evolutionary ecology of offspring quality. Here, we develop a framework to investigate the evolutionary consequences of physiological dynamics by developing theory linking reproductive cell dynamics and components of fitness associated with costly resource allocation decisions to broader life history consequences. We scale these reproductive cell allocation decisions to population‐level survival and fecundity using a life history approach and explore the effects of investment in reproduction or tissue‐specific repair (somatic or reproductive) on the force of selection, reproductive effort, and resource allocation decisions. At the cellular level, we show that investment in protecting reproductive cells increases fitness when reproductive cell maturation rate is high or reproductive cell death is high. At the population level, life history fitness measures show that cellular protection increases reproductive value by differential investment in somatic or reproductive cells and the optimal allocation of resources to reproduction is moulded by this level of investment. Our model provides a framework to understand the evolutionary consequences of physiological processes underlying trade‐offs and highlights the insights to be gained from considering fitness at multiple levels, from cell dynamics through to population growth.     

Variation in lifetime male fitness in Ipomopsis aggregata: tests of sex allocation theory

Sex allocation theory assumes that a shift in allocation of resources to male function both increases male fitness and decreases female fitness. Moreover, the shapes of these fitness gain functions determine whether hermaphroditism or another breeding system is evolutionarily stable. In this article, I first outline information needed to measure these functions in flowering plants. I then use paternity analysis to describe the shapes of the fitness gain functions in natural populations of the hermaphroditic herb Ipomopsis aggregata. I also explore the relationships of male fitness (number of seeds sired) and female fitness (number of seeds produced) to the number of flowers produced by a plant. Plants with greater investment of biomass in the androecium, compared to the gynoecium and seeds, showed increased success at siring seeds, assumed by the models. That sex allocation trait, however, explained only 9% of the variance in estimates of male fitness. The shapes of the fitness gain functions were consistent with theoretical expectations for a hermaphroditic plant, but the model predicted a more female-biased evolutionarily stable strategy (ESS) allocation than was observed. These results lend only partial support the classical sex allocation model.     

Early-late life trade-offs and the evolution of ageing in the wild

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing—the disposable soma and the antagonistic pleiotropy theories—and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.     

A lengthy solution to the optimal propagule size problem in the large-bodied South American freshwater turtle, <Emphasis Type="Italic">Podocnemis unifilis</Emphasis>

In oviparous vertebrates lacking parental care, resource allocation during reproduction is a major maternal effect that may enhance female fitness. In general, resource allocation strategies are expected to follow optimality models to solve the energy trade-offs between egg size and number. Such models predict that natural selection should optimize egg size while egg number is expected to vary with female size, thus maximizing offspring fitness and consequently, maternal fitness. Deviations from optimality predictions are commonly attributed to morphological constraints imposed by female size, such as reported for small-bodied turtle species. However, whether such anatomical constraints exist in smaller-bodied females within large-bodied clades remains unstudied. Here we tested whether resource allocation of the river turtle Podocnemis unifilis (a relatively smaller member of the large-bodied Podocnemididae) follows optimality theory, and found a pattern of egg elongation in smaller females that provides evidence of morphological constraints and of a reproductive trade-off with clutch size, whereas egg width supports the existence of an optimal egg size and no trade-off. Moreover, larger females laid larger clutches composed of rounder eggs, while smaller females laid fewer and relatively more elongated eggs. Elongated eggs from smaller females have larger volume relative to female size and to round eggs of equal width. We propose that elongated eggs represent a solution to a potential morphological constraint suffered by small females. Our results suggest that larger females may optimize fitness by increasing the number of eggs, while smaller females do so by producing larger eggs. Our data supports the notion that morphological constraints are likely more widespread than previously anticipated, such that they may not be exclusive of small-bodied lineages but may also exist in large-bodied lineages.     

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.     

Identifying fitness and optimal life-history strategies for an asexual filamentous fungus

Filamentous fungi are ubiquitous and ecologically important organisms with rich and varied life histories, however, there is no consensus on how to identify or measure their fitness. In the first part of this study we adapt a general epidemiological model to identify the appropriate fitness metric for a saprophytic filamentous fungus. We find that fungal fitness is inversely proportional to the equilibrium density of uncolonized fungal resource patches which, in turn, is a function of the expected spore production of a fungus. In the second part of this study we use a simple life history model of the same fungus within a resource patch to show that a bang-bang resource allocation strategy maximizes the expected spore production, a critical fitness component. Unlike bang-bang strategies identified in other life-history studies, we find that the optimal allocation strategy for saprophytes does not entail the use of all of the resources within a patch.     

A life history model of somatic damage associated with resource acquisition: damage protection or prevention?

A resource acquisition-allocation model is developed to examine the trade-off between reproduction and somatic protection. Unlike previous studies, resource intake is not assumed to be constrained: instead, resource intake is free to vary, with increased intake being associated with an increased risk of somatic damage. This gives rise to an optimal resource intake as well as an optimal allocation strategy. This paper studies the relative importance of acquisition and allocation strategies in regulating acquisition-related mortality. Under the optimal allocation strategy mortality rate increases with age, in accordance with the disposable soma theory of aging. Contrary to the usual interpretation of the disposable soma theory, this increase in mortality can arise from an increase in the resource acquisition effort rather than a decrease in the resources allocated to protection. At early ages resource acquisition is found to be the primary path for regulating life history costs, whilst allocating resources to protection becomes more important later in life. Models for targeted and non-targeted damage repair are considered and the robustness of our results to the structure and parameterization of the model is discussed. The results from our models are discussed in light of published data. Resource acquisition is shown to be a potentially important mechanism for controlling somatic damage which deserves further study.     

Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity

An axiom of life-history theory, and fundamental to our understanding of ageing, is that animals must trade-off their allocation of resources since energy and nutrients are limited. Therefore, animals cannot "have it all"--combine high rates of fecundity with extended lifespans. The idea of life-history trade-offs was recently challenged by the discovery that ageing may be governed by a small subset of molecular processes independent of fitness. We tested the "trade-off" and "having it all" theories by examining the fecundities of C57BL/6J mice placed onto four different dietary treatments that generated caloric intakes from -21 to +8.6% of controls. We predicted body fat would be deposited in relation to caloric intake. Excessive body fat is known to cause co-morbidities that shorten lifespan, while caloric restriction enhances somatic protection and increases longevity. The trade-off model predicts that increased fat would be tolerated because reproductive gain offsets shortened longevity, while animals on a restricted intake would sacrifice reproduction for lifespan extension. The responses of body fat to treatments followed our expectations, however, there was a negative relationship between reproductive performance (fecundity, litter mass) and historical intake/body fat. Our dietary restricted animals had lower protein oxidative damage and appeared able to combine life-history traits in a manner contrary to traditional expectations by having increased fecundity with the potential to have extended lifespans.     

Mate-search efficiency can determine the evolution of separate sexes and the stability of hermaphroditism in animals

Limited availability of mating partners has been proposed as an explanation for the occurrence of simultaneous hermaphroditism in animals with pair mating. When low population density or low mobility of a species limits the number of potential mates, simultaneous hermaphrodites may have a selective advantage because, first, they are able to adjust the allocation of resources between male and female functions in order to maximize fitness; second, in a hermaphroditic population the likelihood of meeting a partner is higher because all individuals are potential mates; and, third, in the absence of mating partners, many simultaneously hermaphroditic animals have the option of reproducing through self-fertilization. Recognizing that mate availability is central to the existing theory of hermaphroditism in animals, it is important to examine the effects of mate search on predictions of the stability of hermaphroditism. Many hermaphroditic animals can increase the number of potential mates they contact by active searching. However, since mate search has costs in terms of time and energy, the increased number of potential mates will be traded off against the amount of resources that can be allocated to the production of gametes. We explore the consequences of this trade-off to the evolution of mating strategies and to the selective advantage of self-fertilization. We show that in low and moderate population densities, poor mate-search efficiency and high costs of searching stabilize hermaphroditism and bias sex allocation toward female function. In addition, in very low population densities, there is strong selective advantage for self-fertilization, but this advantage decreases considerably in species with high mate-search efficiency. Most important, however, we present a novel evolutionary prediction: when mate search is efficient, disruptive frequency-dependent selection on time allocation to mate search leads to the evolution of searching and nonsearching phenotypes and, ultimately, to the evolution of males and females.