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.     

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.     

Sapling structure and regeneration strategy in 18 Shorea species co-occurring in a tropical rainforest

BACKGROUND AND AIMS: Inevitable trade-offs in structure may be a basis for differentiation in plant strategies. Juvenile trees in different functional groups are characterized by specific suites of structural traits such as crown architecture and biomass distribution. The relationship between juvenile tree structure and function was tested to find out if it is robust among functionally and taxonomically similar species of the genus Shorea that coexist sympatrically in a tropical rain forest in Borneo. METHODS: The sapling structures of 18 species were compared for standardized dry masses of 5 and 30 g. Pairwise simple correlation and multiple correlation patterns among structural traits of juveniles (0.1-1.5 m in height) of 18 Shorea species were examined using Pearson's correlation and principal component analysis (PCA), respectively. The correlation was then tested between the PCA results and three indices of shade tolerance: the net photosynthetic rate, the wood density of mature trees and seed size. KEY RESULTS: The structural variation in saplings of the genus Shorea was as large as that found in sets of species with much more diverse origins. The PCA showed that both crown architecture and allocation to leaves are major sources of variation in the structures of the 18 species investigated. Of these two axes, allocation to leaves was significantly correlated with wood density and showed a limited correlation with photosynthetic rate, whereas crown architecture was significantly correlated to seed size. CONCLUSIONS: Overall, the results suggest that an allocation trade-off between leaves and other organs, which co-varied with wood density and to a certain extent with photosynthetic capacity, accounts for the difference in shade tolerance among congeneric, functionally similar species. In contrast, the relationship between the architecture and regeneration strategy differed from the pattern found between functional groups, and the function of crown architecture was ambiguous.     

Trade-off acquisition and allocation in Gryllus firmus: a test of the Y model

Many models of life history evolution assume trade-offs between major life history traits; however, these trade-offs are often not found. The Y model predicts that variation in acquisition can mask underlying allocation trade-offs and is a major hypothesis explaining why negative relationships are not always found between traits that are predicted to trade-off with one another. Despite this model's influence on the field of life history evolution, it has rarely been properly tested. We use a model system, the wing dimorphic cricket, Gryllus firmus as a case study to test the assumptions and predictions of the Y model. By experimentally altering the acquisition regime and by estimating energy acquisition and energy allocation directly in this species, we are able to explicitly test this important model. Overall, we find strong support for the predictions of the Y model.     

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.     

Exploration or exploitation: life expectancy changes the value of learning in foraging strategies

The acquisition of information is a fundamental part of individual foraging behaviour in heterogeneous and changing environments. We examine how foragers may benefit from utilizing a simple learning rule to update estimates of temporal changes in resource levels. In the model, initial expectation of resource conditions and rate of replacing past information by new experiences are genetically inherited traits. Patch-time allocation differs between learners and foragers that use a fixed patch-leaving threshold throughout the foraging season. It also deviates from foragers that obtain information about the environment at no cost. At the start of a foraging season, learners sample the environment by frequent movements between patches, sacrificing current resource intake for information acquisition. This is done to obtain more precise and accurate estimates of resource levels, resulting in increased intake rates later in season. Risk of mortality may alter the trade-off between exploration and exploitation and thus change patch sampling effort. As lifetime expectancy decreases, learners invest less in information acquisition and show lower foraging performance when resource level changes through time.     

Estimating age at maturation and energy-based life-history traits from individual growth trajectories with nonlinear mixed-effects models

A new method is presented to estimate individuals’ (1) age at maturation, (2) energy acquisition rate, (3) energy expenditure for body maintenance, and (4) reproductive investment, and the multivariate distribution of these traits in a population. The method relies on adjusting a conceptual energy allocation model to individual growth curves using nonlinear mixed-effects modelling. The method’s performance was tested using simulated growth curves for a range of life-history types. Individual age at maturation, energy acquisition rate and the sum of maintenance and reproductive investment rates, and their multivariate distribution, were accurately estimated. For the estimation of maintenance and reproductive investment rates separately, biases were observed for life-histories with a large imbalance between these traits. For low reproductive investment rates and high maintenance rates, reproductive investment rate estimates were strongly biased whereas maintenance rate estimates were not, the reverse holding in the opposite situation. The method was applied to individual growth curves back-calculated from otoliths of North Sea plaice (Pleuronectes platessa) and from scales of Norwegian spring spawning herring (Clupea harengus). For plaice, maturity ogives derived from our individual estimates of age at maturation were almost identical to the maturity ogives based on gonad observation in catch samples. For herring, we observed 51.5 % of agreement between our individual estimates and those directly obtained from scale reading, with a difference lower than 1 year in 97 % of cases. We conclude that the method is a powerful tool to estimate the distribution of correlated life-history traits for any species for which individual growth curves are available.     

Experimental tests of sex-allocation theory in plants

A general explanation for diversity in plant breeding systems is offered by sex-allocation theory. This theory assumes a trade-off between allocation of resources to the two sexual functions. It explains the high frequency of hermaphroditism in angiosperms by diminishing fitness returns on investment of more resources in a single function. Recent experimental studies provide tests of this theory by measuring male and female fitness gains, and examining the trade-off assumption. These studies show how fitness responds to shifts in allocation. Allocation traits often show heritable variation, but support for a trade-off remains weak.     

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.     

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.     

The plant traits that drive ecosystems: Evidence from three continents

Question: A set of easily‐measured (‘soft’) plant traits has been identified as potentially useful predictors of ecosystem functioning in previous studies. Here we aimed to discover whether the screening techniques remain operational in widely contrasted circumstances, to test for the existence of axes of variation in the particular sets of traits, and to test for their links with ‘harder’ traits of proven importance to ecosystem functioning. Location: central‐western Argentina, central England, northern upland Iran, and north‐eastern Spain. Recurrent patterns of ecological specialization: Through ordination of a matrix of 640 vascular plant taxa by 12 standardized traits, we detected similar patterns of specialization in the four floras. The first PCA axis was identified as an axis of resource capture, usage and release. PCA axis 2 appeared to be a size‐related axis. Individual PCA for each country showed that the same traits remained valuable as predictors of resource capture and utilization in all of them, despite their major differences in climate, biogeography and land‐use. The results were not significantly driven by particular taxa: the main traits determining PCA axis 1 were very similar in eudicotyledons and monocotyledons and Asteraceae, Fabaceae and Poaceae. Links between recurrent suites of ‘soft’ traits and ‘hard’ traits: The validity of PCA axis 1 as a key predictor of resource capture and utilization was tested by comparisons between this axis and values of more rigorously established predictors (‘hard’ traits) for the floras of Argentina and England. PCA axis 1 was correlated with variation in relative growth rate, leaf nitrogen content, and litter decomposition rate. It also coincided with palatability to model generalist herbivores. Therefore, location on PCA axis 1 can be linked to major ecosystem processes in those habitats where the plants are dominant. Conclusion: We confirm the existence at the global scale of a major axis of evolutionary specialization, previously recognised in several local floras. This axis reflects a fundamental trade‐off between rapid acquisition of resources and conservation of resources within well‐protected tissues. These major trends of specialization were maintained across different environmental situations (including differences in the proximate causes of low productivity, i.e. drought or mineral nutrient deficiency). The trends were also consistent across floras and major phylogenetic groups, and were linked with traits directly relevant to ecosystem processes.     

Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird

Why do animals not grow at their maximal rates? It has been recently proposed that fast growth leads to the accumulation of cellular damages due to oxidative stress, influencing subsequent performances and life span. Therefore, the trade-off between fast growth and oxidative stress may potentially function as an important constraint in the evolution of growth trajectories. We test this by examining a potential antagonistic pleiotropy between growth and blood resistance to controlled free radical attack in a wild bird using a cross-fostering design and robust quantitative genetic analyses. In the yellow-legged gull Larus michahellis, decreased resistance to oxidative stress at age 8 days was associated with faster growth in mass, across the first 8 days of life, suggesting a trade-off between mass growth and oxidative-stress-related somatic maintenance. We found a negative genetic correlation between chick growth and resistance to oxidative stress, supporting the presence of the genetic trade-off between the two traits. Therefore, investment of somatic resources in growth could be constrained by resistance to oxidative stress in phenotypic and genetic levels. Our results provide first evidence for a potential genetic trade-off between life-history and underlying physiological traits in a wild vertebrate. Future studies should explore genetic trade-offs between life-history traits and other oxidative-stress-related traits.     

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.     

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.     

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.     

Context-dependent development of sexual ornamentation: implications for a trade-off between current and future breeding efforts

Allocation of resources into the development of sexual displays is determined by a trade-off between the competing demands of current reproduction and self-maintenance. When reproduction overlaps with acquisition of sexual ornamentation, such as in birds with a yearly post-breeding moult, such a trade-off can be expressed in elaboration of sexual traits used in subsequent matings. In turn, selection for elaboration of sexual ornaments should favour resolution of this trade-off through a modification of the ornaments' development, resulting in variable and life history-dependent development of sexual displays. Here we examined a novel hypothesis that the trade-off between current reproduction and development of sexual ornamentation in the house finch (Carpodacus mexicanus) can be mediated by the shared effects of prolactin - a pituitary hormone that regulates both parental care and moult in this species. We compared developmental variation in sexual ornamentation between breeding, nonbreeding, and juvenile males and examined the relative contribution of residual levels of prolactin and individual condition during moult to the acquisition of sexual ornamentation. Males that invested heavily in parental care entered post-breeding moult in lower condition and later in the season, but their higher plasma prolactin was associated with shorter and more intense moult ultimately resulting in equal or greater elaboration of sexual ornamentation compared with nonparental males. Elaboration of sexual ornamentation of nonparental males that entered moult in greater condition, but with lower prolactin, was produced by longer and earlier moult and by lesser overlap in moult between sexual ornaments. Ornamentation of juvenile males that acquire sexual ornamentation for the first time was closely associated with physiological condition during moult. We discuss the implications of such context-dependent ontogenies of sexual ornamentation and resulting differences in condition-dependence of sexual traits across life history stages on the evolution of female preference for elaborated sexual displays.     

Condition dependence and trade-offs of sexual versus non-sexual traits in an insect

Sexual traits often communicate male condition and so are known to be highly condition-dependent. Thus, it is expected that, under restricted environments, sexual traits will be more heavily impacted than non-sexual traits, and so a negative covariation will be expected between sexual traits and non-sexual traits as only high-quality males will sustain the costs of producing both trait types. Such covariation will not necessarily appear in non-restricted environments. We tested these predictions using males of the American rubyspot, Hetaerina americana. First, fully mature males from different seasons were collected and their sexual [a wing red spot and body size (this corrected for body mass using residuals)], and condition-indicating, non-sexual (phenoloxidase and protein concentration) traits were measured. Second, larvae were reared under different food quantities and the same traits plus another non-sexual trait [pro-phenoloxidase (proPO)], were measured in recently emerged males. Contrary to expected, non-sexual traits showed larger expression variance than sexual traits. We found a significant covariation between body size and proPO for experimental males. Both rich and poor diet groups showed a negative slope for body size and proPO. This supposes a resource allocation trade-off between these two traits for recently emerged animals. On the other hand, the presumed signaling function between sexual traits, such as spot size, and physiological indicators of condition in this species, is not supported.     

Constraints on plant signals and rewards to multiple mutualists?

Many plants invest substantial resources in signaling to and rewarding two kinds of ‘interguild’ mutualists, pollinators and seed dispersers. The signals and rewards are expressed via traits of flowers and fruits. Pollinators and seed dispersers could act in synergistic or antagonistic ways to influence selection on these traits. Here, we address the issue of whether plant species might be constrained in signaling to and rewarding multiple mutualists that provide different types of benefits to plants. Specifically, does investment in one type of mutualist limit investment in another? We examined the correlation between flower size and fruit size for 472 plant species spanning three regional floras. Our analyses made the assumption that structure size is related to plant investment in signals and/or rewards. We expect that a constraint due to interguild mutualisms would be evidenced by a negative correlation between flower and fruit size. Instead, we found significantly positive relationships between flower size and fruit size in all three regional floras. These relationships remained robust after correcting for plant evolutionary history using phylogenetically independent contrasts. These patterns may reflect synergies in selection by pollinators and seed dispersers, genetically-based or resource-based constraints on investment in reproductive tissues, and/or an underlying trade-off in structure size versus number.     

Path analysis of the genetic integration of traits in the sand cricket: a novel use of BLUPs

This study combines path analysis with quantitative genetics to analyse a key life history trade-off in the cricket, Gryllus firmus. We develop a path model connecting five traits associated with the trade-off between flight capability and reproduction and test this model using phenotypic data and estimates of breeding values (best linear unbiased predictors) from a half-sibling experiment. Strong support by both types of data validates our causal model and indicates concordance between the phenotypic and genetic expression of the trade-off. Comparisons of the trade-off between sexes and wing morphs reveal that these discrete phenotypes are not genetically independent and that the evolutionary trajectories of the two wing morphs are more tightly constrained to covary than those of the two sexes. Our results illustrate the benefits of combining a quantitative genetic analysis, which examines statistical correlations between traits, with a path model that focuses upon the causal components of variation.     

Distribution of functional traits in subtropical trees across environmental and forest use gradients

The relationship between functional traits and environmental factors contribute to understanding community structure and predicting which species will be able to elude environmental filters in different habitats. We selected 10 functional traits related to morphology, demography and regeneration niche in 54 subtropical premontane tree species to describe their main axes of functional differentiation. We derived species traits, environmental variables and species abundance data from 20 1-ha permanent plots established in a seasonal subtropical premontane forest in northwestern Argentina. We analyzed the relationship between species functional traits and environmental factors through RLQ and fourth-corner analyzes. We found an axis of structural differentiation that segregates understory from canopy species, and an axis of functional differentiation that segregates species that maximize resource acquisition from those that promote resource conservation. Environmental and forest use gradients operate hierarchically over subtropical premontane tree species influencing the distribution of demographic and morphological traits. The interaction between climatic and topographic factors influences the distribution of species functional traits at the regional scale. In addition, the history of forest use seems to operate at the landscape scale and explains the distribution of species traits reflecting a trade-off between resource acquisition and resource conservation strategies in secondary forests across different successional stages. Our results support the idea that functional traits may be used to analyze community structure and dynamics through niche differentiation and environmental filtering processes.