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.     

Architectural Tradeoffs between Adventitious and Basal Roots for Phosphorus Acquisition

Adventitious rooting contributes to efficient phosphorus acquisition by enhancing topsoil foraging. However, metabolic investment in adventitious roots may retard the development of other root classes such as basal roots, which are also important for phosphorus acquisition. In this study we quantitatively assessed the potential effects of adventitious rooting on basal root growth and whole plant phosphorus acquisition in young bean plants. The geometric simulation model SimRoot was used to dynamically model root systems with varying architecture and C availability growing for 21 days at 3 planting depths in 3 soil types with contrasting nutrient mobility. Simulated root architectures, tradeoffs between adventitious and basal root growth, and phosphorus acquisition were validated with empirical measurements. Phosphorus acquisition and phosphorus acquisition efficiency (defined as mol phosphorus acquired per mol C allocated to roots) were estimated for plants growing in soil in which phosphorus availability was uniform with depth or was greatest in the topsoil, as occurs in most natural soils. Phosphorus acquisition and acquisition efficiency increased with increasing allocation to adventitious roots in stratified soil, due to increased phosphorus depletion of surface soil. In uniform soil, increased adventitious rooting decreased phosphorus acquisition by reducing the growth of lateral roots arising from the tap root and basal roots. The benefit of adventitious roots for phosphorus acquisition was dependent on the specific respiration rate of adventitious roots as well as on whether overall C allocation to root growth was increased, as occurs in plants under phosphorus stress, or was lower, as observed in unstressed plants. In stratified soil, adventitious rooting reduced the growth of tap and basal lateral roots, yet phosphorus acquisition increased by up to 10% when total C allocation to roots was high and adventitious root respiration was similar to that in basal roots. With C allocation to roots decreased by 38%, adventitious roots still increased phosphorus acquisition by 5%. Allocation to adventitious roots enhanced phosphorus acquisition and efficiency as long as the specific respiration of adventitious roots was similar to that of basal roots and less than twice that of tap roots. When adventitious roots were assigned greater specific respiration rates, increased adventitious rooting reduced phosphorus acquisition and efficiency by diverting carbohydrate from other root types. Varying the phosphorus diffusion coefficient to reflect varying mobilities in different soil types had little effect on the value of adventitious rooting for phosphorus acquisition. Adventitious roots benefited plants regardless of basal root growth angle. Seed planting depth only affected phosphorus uptake and efficiency when seed was planted below the high phosphorus surface stratum. Our results confirm the importance of root respiration in nutrient foraging strategies, and demonstrate functional tradeoffs among distinct components of the root system. These results will be useful in developing ideotypes for more nutrient efficient crops.     

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.     

Sub-Optimal Allocation of Time in Sequential Movements

The allocation of limited resources such as time or energy is a core problem that organisms face when planning complex actions. Most previous research concerning planning of movement has focused on the planning of single, isolated movements. Here we investigated the allocation of time in a pointing task where human subjects attempted to touch two targets in a specified order to earn monetary rewards. Subjects were required to complete both movements within a limited time but could freely allocate the available time between the movements. The time constraint presents an allocation problem to the subjects: the more time spent on one movement, the less time is available for the other. In different conditions we assigned different rewards to the two tokens. How the subject allocated time between movements affected their expected gain on each trial. We also varied the angle between the first and second movements and the length of the second movement. Based on our results, we developed and tested a model of speed-accuracy tradeoff for sequential movements. Using this model we could predict the time allocation that would maximize the expected gain of each subject in each experimental condition. We compared human performance with predicted optimal performance. We found that all subjects allocated time sub-optimally, spending more time than they should on the first movement even when the reward of the second target was five times larger than the first. We conclude that the movement planning system fails to maximize expected reward in planning sequences of as few as two movements and discuss possible interpretations drawn from economic theory.     

Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history

Acquisition and allocation of resources are central to life‐history theory. However, empirical work typically focuses only on allocation despite the fact that relationships between fitness components may be governed by differences in the ability of individuals to acquire resources across environments. Here, we outline a statistical framework to partition the genetic basis of multivariate plasticity into independent axes of genetic variation, and quantify for the first time, the extent to which specific traits drive multitrait genotype–environment interactions. Our framework generalises to analyses of plasticity, growth and ageing. We apply this approach to a unique, large‐scale, multivariate study of acquisition, allocation and plasticity in the life history of the cricket, Gryllus firmus. We demonstrate that resource acquisition and allocation are genetically correlated, and that plasticity in trade‐offs between allocation to components of fitness is 90% dependent on genetic variance for total resource acquisition. These results suggest that genotype–environment effects for resource acquisition can maintain variation in life‐history components that are typically observed in the wild.     

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.     

Outcrossing hermaphroditic polychaete worms adjust their sex allocation to social conditions

Sex allocation theory predicts that simultaneous hermaphrodites shift sex allocation facultatively in response to variation in local group size. This study was performed to evaluate the relative investment in each sex function by the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema and to test whether allocation to each sex depends on the number of reproductive competitors. Four experimental groups were set up (in a 2 x 2 factorial design) with small or large group size and with small or large enclosures to control for potential confounding effects of density. We measured the proportion of female and male investment in focal individuals. Results revealed that individuals regulated their reproductive output so that when reproductive competitors were present, the number of female gametes was strongly reduced and the male function increased. In contrast, under monogamy, individuals in small groups produced lower numbers of sperm but had a higher egg output than worms in large groups. Density did not affect sex allocation in our experiment. Our findings provide qualitative support for Local Mate Competition theory, but also show that the pattern of sex allocation specific to this species is more complex than expected by current theory.     

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.     

Trade-offs between reproductive and somatic (storage) investments in animals: a comparative test of the Van Noordwijk and De Jong model

Classical life-history theory predicts ‘trade-offs’ between reproductive and somatic investments. However, empirical studies have shown that intraspecific phenotypic correlations between these two resource investments are often positive or nonsignificant, rather than negative as predicted. The model of Van Noordwijk and De Jong (1986) was proposed to explain these unexpected results. According to their model, positive correlations between reproductive and somatic investments will result if individual variation in resource acquisition exceeds that of resource allocation, whereas negative correlations will result if individual variation in resource allocation exceeds that of resource acquisition. To test this model, I used body storage/condition as an index of somatic investment because it is usually strongly related to level of resource acquisition. I predicted that laboratory studies should more often show negative correlations between reproductive and somatic investments than field studies, because individual variation in resource acquisition is expected to be lower in controlled laboratory environments than in variable natural environments. A literature review revealed that correlations between somatic (storage) investment and reproductive investment (estimated as clutch/litter mass, number of offspring per clutch/litter, or number of clutches/litters) among conspecific breeding female animals are more often positive (15 species) or nonsignificant (17 species) than negative (6 species). Moreover, as expected, five of six negative correlations were observed in laboratory studies, whereas 13 of 15 positive correlations were observed in field studies. It is concluded that future empirical and theoretical work on life histories should consider individual variation in both resource acquisition and allocation and the interaction between the two. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Optimal vaccine allocation for COVID-19 in the Netherlands: A data-driven prioritization

For the control of COVID-19, vaccination programmes provide a long-term solution. The amount of available vaccines is often limited, and thus it is crucial to determine the allocation strategy. While mathematical modelling approaches have been used to find an optimal distribution of vaccines, there is an excessively large number of possible allocation schemes to be simulated. Here, we propose an algorithm to find a near-optimal allocation scheme given an intervention objective such as minimization of new infections, hospitalizations, or deaths, where multiple vaccines are available. The proposed principle for allocating vaccines is to target subgroups with the largest reduction in the outcome of interest. We use an approximation method to reconstruct the age-specific transmission intensity (the next generation matrix), and express the expected impact of vaccinating each subgroup in terms of the observed incidence of infection and force of infection. The proposed approach is firstly evaluated with a simulated epidemic and then applied to the epidemiological data on COVID-19 in the Netherlands. Our results reveal how the optimal allocation depends on the objective of infection control. In the case of COVID-19, if we wish to minimize deaths, the optimal allocation strategy is not efficient for minimizing other outcomes, such as infections. In simulated epidemics, an allocation strategy optimized for an outcome outperforms other strategies such as the allocation from young to old, from old to young, and at random. Our simulations clarify that the current policy in the Netherlands (i.e., allocation from old to young) was concordant with the allocation scheme that minimizes deaths. The proposed method provides an optimal allocation scheme, given routine surveillance data that reflect ongoing transmissions. This approach to allocation is useful for providing plausible simulation scenarios for complex models, which give a more robust basis to determine intervention strategies.     

Conflict over sex allocation drives conflict over reproductive allocation in perennial social insect colonies

Queen-worker conflict in the social Hymenoptera has become a cornerstone of sex-ratio theory. Extending that theory to conflict over life-history decisions, however, has proven controversial. Pamilo first proposed that queen-worker conflict over reproductive allocation should be important in perennial, social insect colonies, but Bourke and Chan have questioned the generality of that claim. Here, we reexamine this problem for the simplest case of a monogynous and monandrous hymenopteran society by relaxing assumptions of Pamilo's model. In populations with monomorphic sex ratios, queens and workers agree on allocation to growth versus reproduction. However, variation in sex allocation across colonies can induce queen-worker conflict over reproductive allocation; the former is a necessary condition for the latter. We explore how conflict over reproductive allocation depends on the population-wide sex ratio, the survivorship probabilities for existing colonies, and the likelihood of establishing new colonies. We then test our theory for two ant species, each with two years of data. We find considerable support for our contention of queen-worker conflict over reproductive allocation and suggest how future studies should be structured to explore this conflict further.     

Intraspecific variation in sex allocation in hermaphroditic Plantago coronopus (L.)

Models for sex allocation assume that increased expenditure of resources on male function decreases the resources available for female function. Under some circumstances, a negative genetic correlation between investment in stamens and investment in ovules or seeds is expected. Moreover, if fitness returns for investment in male and female function are different with respect to size, sex allocation theory predicts size‐specific gender changes. We studied sex allocation and genetic variation for investment in stamens, ovules and seeds at both the flower and the plant level in a Dutch population of the wind‐pollinated and predominantly outcrossing Plantago coronopus. Data on biomass of floral structures, stamens, ovules, seedset and seedweight were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and (genetic) correlations were estimated from the greenhouse‐grown progeny of maternal families, raised at two nutrient levels. The proportion of reproductive biomass invested in male function was high at flowering (0.86 at both nutrient levels) and much lower at fruiting (0.30 and 0.40 for the high and low nutrient treatment, respectively). Androecium and gynoecium mass exhibited moderately high levels of genetic variance, with broad‐sense heritabilities varying from 0.35 to 0.56. For seedweight no genetic variation was detected. Significant among‐family variation was also detected for the proportion of resources invested in male function at flowering, but not at fruiting. Phenotypic and broad‐sense genetic correlations between androecium and gynoecium mass were positive. Even after adjusting for plant size, as a measure of resource acquisition, maternal families that invested more biomass in the androecium also invested more in the gynoecium. This is consistent with the hypothesis that genetic variation for resource acquisition may in part be responsible for the overall lack of a negative correlation between male and female function. Larger plants had a more female‐biased allocation pattern, brought about by an increase in seedset and seedweight, whereas stamen biomass did not differ between small and large plants. These results are discussed in relation to size‐dependent sex allocation theory (SDS). Our results indicate that the studied population harboured substantial genetic variation for reproductive characters.     

The type and timing of social information alters offspring production

The acquisition and use of information are essential for decision-making in an uncertain world. The use of social information, or information from the behaviour of others, may be a common and efficient mechanism to improve estimates of resource quality by animals. According to theory, social information cues with higher information content should have a greater influence on decision-making, and current information should be weighed more than prior information. However, experimental tests of these hypotheses remain scarce. We exposed female cactus bugs (Chelinidea vittiger) to different types of social information (the presence of conspecific eggs or nymphs) presented at different times (current or prior to egg laying) to determine the influence of social information on offspring production. We found that social information substantially altered the number of eggs produced. The presence of conspecific eggs, regardless of timing, consistently increased egg production, whereas nymphs only increased egg production when present during egg laying. We conclude that the type and timing of social information may have an important, yet unappreciated, influence on reproductive allocation.     

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.     

C allocation to the fungus is not a cost to the plant in ectomycorrhizae

Mycorrhizal benefit to plants is most frequently evaluated through growth differences between mycorrhizal (M) and non‐mycorrhizal (NM) plants. These growth differences are often considered to be due to differences in belowground C expenditure, or in cost efficiency, i.e. amount of nutrients acquired per C expended. We searched published reports for relations between plant growth and belowground C allocation, C use efficiency, or nutrient uptake, in ectomycorrhizal (ECM) versus non‐mycorrhizal plants. We found a similar number of cases of negative, null or positive effects of ECM on plant growth. These effects were not correlated with differences on belowground C allocation or C use efficiency between M and NM plants. In contrast, they were very strongly correlated with mycorrhizal effects on plant N gain. A comprehensive analysis of the published data therefore provided evidence that C is an excess, rather than a costly, resource, and that the outcome of the symbiosis depends only on whether mycorrhizae result in increased or decreased nutrient acquisition compared with NM plants, and not on cost efficiency differences between M and NM plants. Consequences of this finding for the regulation of resource exchange between symbionts and the nature of the symbiosis are discussed.     

A Dynamic Energy Budget model based on partitioning of net production

We formulate a Dynamic Energy Budget (DEB) model for the growth and reproduction of individual organisms based on partitioning of net production (i.e. energy acquisition rate minus maintenance rate) between growth and energy reserves. Reproduction uses energy from reserves. The model describes both feeding and non-feeding stages, and hence is applicable to embryos (which neither feed nor reproduce), juveniles (which feed but do not reproduce), and adults (which commonly both feed and reproduce). Embryonic growth can have two forms depending on the assumptions for acquisition of energy from yolk. By default, when the energy acquisition rate exceeds the maintenance rate, a fixed proportion of the resulting net production is spent on growth (increase in structural biomass), and the remaining portion is channelled to the reserves. Feeding organisms, however, modulate their allocation of net production energy in response to their total energy content (energy in the reserves plus energy bounded to structural biomass). In variable food environment an organism alternates between periods of growth, no-growth, and balanced-growth. In the latter case the organism adopts an allocation strategy that keeps its total energy constant. Under constant environmental conditions, the growth of a juvenile is always of von Bertalanffy type. Depending on the values of model parameters there are two long-time possibilities for adults: (a) von Bertalanffy growth accompanied by reproduction at a rate that approaches zero as the organism approaches asymptotic size, or (b) abrupt cessation of growth at some finite time, following which, the rate of reproduction is constant. We illustrate the model's applicability in life history theory by studying the optimum values of the energy allocation parameters for constant environment and for each of the dynamic regimes described above. Received: 11 May 1998 / Revised version: 18 February 2000 / Published online: 4 October 2000     

Carbon allocation in fruit trees: from theory to modelling

Carbon allocation within a plant depends on complex rules linking source organs (mainly shoots) and sink organs (mainly roots and fruits). The complexity of these rules comes from both regulations and interactions between various plant processes involving carbon. This paper presents these regulations and interactions, and analyses how agricultural management can influence them. Ecophysiological models of carbon production and allocation are good tools for such analyses. The fundamental bases of these models are first presented, focusing on their underlying processes and concepts. Different approaches are used for modelling carbon economy. They are classified as empirical, teleonomic, driven by source–sink relationships, or based on transport and chemical/biochemical conversion concepts. These four approaches are presented with a particular emphasis on the regulations and interactions between organs and between processes. The role of plant architecture in carbon partitioning is also discussed and the interest of coupling plant architecture models with carbon allocation models is highlighted. As an illustration of carbon allocation models, a model developed for peach trees, describing carbon transfer within the plant, and based on source–sink and Münch transport theory is presented and used for analyzing the link between roots, shoots and reproductive compartments. On this basis, the consequences of fruit load or plant pruning on fruit and vegetative growth can be evaluated.     

Fine Root Growth Increases in Response to Nitrogen Addition in Phosphorus-limited Northern Hardwood Forests

Ecosystems - Resource allocation theory posits that increased soil nutrient availability results in decreased plant investment in nutrient acquisition. We evaluated this theory by quantifying fine...     

Will male advertisement be a reliable indicator of paternal care,if offspring survival depends on male care?

Existing theory predicts that male signalling can be an unreliable indicator of paternal care, but assumes that males with high levels of mating success can have high current reproductive success, without providing any parental care. As a result, this theory does not hold for the many species where offspring survival depends on male parental care. We modelled male allocation of resources between advertisement and care for species with male care where males vary in quality, and the effect of care and advertisement on male fitness is multiplicative rather than additive. Our model predicts that males will allocate proportionally more of their resources to whichever trait (advertisement or paternal care) is more fitness limiting. In contrast to previous theory, we find that male advertisement is always a reliable indicator of paternal care and male phenotypic quality (e.g. males with higher levels of advertisement never allocate less to care than males with lower levels of advertisement). Our model shows that the predicted pattern of male allocation and the reliability of male signalling depend very strongly on whether paternal care is assumed to be necessary for offspring survival and how male care affects offspring survival and male fitness.