Plasticity in resource allocation based life history traits in the Pacific oyster, Crassostrea gigas. I. Spatial variation in food abundance

We investigated the quantitative genetics of plasticity in resource allocation between survival, growth and reproductive effort in Crassostrea gigas when food abundance varies spatially. Resource allocation shifted from survival to growth and reproductive effort as food abundance increased. An optimality model suggests that this plastic shift may be adaptive. Reproductive effort plasticity and mean survival were highly heritable, whereas for growth, both mean and plasticity had low heritability. The genetic correlations between reproductive effort and both survival and growth were negative in poor treatments, suggesting trade-offs, but positive in rich ones. These sign reversals may reflect genetic variability in resource acquisition, which would only be expressed when food is abundant. Finally, we found positive genetic correlations between reproductive effort plasticity and both growth and survival means. The latter may reflect adaptation of C. gigas to differential sensitivity of fitness to survival, such that genetic variability in survival mean might support genetic variability in reproductive effort plasticity.     

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.     

Evolutionary responses of Drosophila melanogaster to selection at different larval densities: changes in genetic variation,specialization and phenotypic plasticity

Abstract We studied the evolutionary response to novel environments by applying artificial selection for total progeny biomass in populations of Drosophila melanogaster maintained at three different larval population densities. We found the relative amount of genetic variability for characters related with biomass to be lower and the correlation between them more negative at the intermediate density, and that selection resulted in changes in phenotypic plasticity and in patterns of resource allocation between traits. We found some evidence for tradeoffs between densities, which suggests that populations living at heterogeneous densities might be subject to disruptive selection. Our results show that adaptation to new environments may be a complex process, involving not only changes in trait means, but also in correlations between traits and between environments.     

Geographic variation in primary sex allocation per flower within and among 12 species of Pedicularis (Orobanchaceae): Proportional male investment increases with elevation

? Premise of the study: The study of geographic variation in ecologically important traits within and among taxa is a first step toward understanding the environmental factors that contribute to population differentiation and species divergence. This study examines variation in mean sex allocation per flower (androecium mass/gynoecium mass) among 49 wild populations representing 12 Pedicularis species across an elevation gradient on the eastern Tibetan Plateau. ? Methods: We used population means to evaluate sources of variation in per-flower sex allocation within and across species. In particular, we evaluate the relative influence of intrinsic (i.e., plant size, estimated as aboveground stem biomass) vs. extrinsic factors affecting mean sex allocation among populations. ? Key results: Mean sex allocation per flower (the relative investment in male floral organs) is negatively correlated with mean plant size; populations of large plants produce relatively female-biased flowers. This relationship between mean plant size and mean sex allocation is not statistically significant, however, when the effect of elevation is controlled statistically. Among populations within and across species, mean sex allocation increases with elevation. This relationship persists even when the effect of mean plant size is controlled statistically. Factors associated with increasing elevation appear to favor genotypes and/or taxa with male-biased flowers. ? Conclusion: Extrinsic environmental conditions may be more important than intrinsic resource status in determining patterns of geographic variation in mean sex allocation among populations or species of Pedicularis. We cannot conclude whether the effect of elevation on mean sex allocation is the result of environmentally induced plasticity, genetically based adaptation, or species sorting, but it is only partly mediated by mean plant size.     

Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water,nutrient and light gradients

The univariate and multivariate study of variation for phenotypic plasticity is central to providing a clear understanding of hypotheses about the genetic control and evolution of reaction norms in natural populations. Arabidopsis thaliana is an ideal organism for the study of Genotype × Environment interactions (i.e., genetic variation for plasticity), because of the ease with which it can be grown in large numbers and due to the amount of information already available on its genetics, physiology and developmental biology. In this paper, we report on the plasticity, genetic variation and G × E interactions of four populations of A. thaliana in response to three environmental gradients (water, light and nutrients), each characterized by four levels of the controlled parameter. We measured nine traits and obtained their reaction norms. Path analysis was used to study the plasticity of character correlations. We found a tendency for A. thaliana reaction norms to be linear (either flat, i.e. no plasticity, or with a significant slope), in accordance with previous studies. We detected substantial amounts of genetic variation for plasticity in the light and nutrient gradients, but not in the water gradient. Dramatic restructuring of character correlations was induced by changes in environmental conditions, although some paths tended to be stable irrespective of the environment, thereby suggesting some degree of canalization.     

Population differentiation in climate sensitivity of resin duct formation during growth resumption in Pinus pinaster

To counteract the effects of herbivores and pathogens, conifers have developed a sophisticated resin-based defensive system. Since defences are costly, trees must continuously accommodate defensive investment throughout plastic responses to environmental stimuli. However, the extent of such responses can differ at the intra-specific level (i.e. genetic variation in plasticity). Here we examined whether and to what extent year-to-year climate fluctuations, an important source of environmental heterogeneity during the trees' life, drive plasticity in defensive allocation of a widespread pine species. Specifically, we quantified interannual variation in resin duct production along a 31-year-period in 174 Pinus pinaster trees of nine range-wide populations grown in two common gardens in Central Spain. We aimed to explore (i) patterns of interannual variation (i.e., temporal plasticity) in resin duct production among populations and sites, (ii) whether such patterns are linked to plastic responses to interannual variation in climate conditions (i.e., climatic plasticity), and (iii) whether plastic responses to climate differ among populations (i.e., genetic variation in plasticity) and sites. We found large interannual plasticity in resin duct production (22.8 % of total variance), with temporal patterns differing among sites and populations. Climate conditions during the early growth period significantly affected the annual differentiation of resin ducts. Particularly, April precipitation had a positive overall effect on resin duct production. Inversely, warmer conditions in April had a negative effect but only in certain populations, which demonstrates genetic variation in climate sensitivity of resin duct formation. Despite significant effects of certain climate variables on annual resin duct production, climate only accounted for a small proportion of the total interannual variation (up to 3.8 % of interannual variation explained by climate factors). This suggests that alternative factors such as trade-offs with growth and temporal variation in biotic and non-climatic abiotic conditions likely contribute to explain interannual fluctuations in defensive investment.     

Plasticity and ontogenetic drift of biomass allocation in response to above- and below-ground resource availabilities in perennial herbs: a case study of <Emphasis Type="Italic">Alternanthera philoxeroides</Emphasis>

Changes in plant biomass allocation in response to varying resource availabilities may result from ontogenetic drift caused by allometric growth (i.e., apparent plasticity), a true adjustment of ontogenetic trajectories (true plasticity) or both (complex plasticity). Given that the root allocation of annual species usually decreases during the growth, the developmentally explicit model predicts that annual herbs will exhibit true plasticity in root allocation under above-ground resource limitation and apparent plasticity for moderate stress of below-ground resource. For perennial species, the root allocation of which increases during growth, the reverse patterns would be expected. In this study, we tested the developmentally explicit model with a perennial weed, Alternanthera philoxeroides (Mart.) Griseb. We report its adaptive changes and ontogenetic drift of root allocation in response to different resource levels (i.e., light, water and nutrient availability) by comparing root allocation on both an age and a size basis. The root allocation of A. philoxeroides increased with the size (i.e., ontogenetic drift) during the growth, and exhibited significant changes in response to different resource availabilities. Furthermore, the root allocation in response to water or nutrient availability exhibited typical complex plasticity, while the light stress only slowed down the growth, with the ontogenetic trajectory unchanged (apparent plasticity). The contrasting responses to above-ground and below-ground stresses were consistent with the prediction of the developmentally explicit model.     

Coevolution between parasite virulence and host life-history traits

Epidemiological models generally explore the evolution of parasite life-history traits, namely, virulence and transmission, against a background of constant host life-history traits. However, life-history models have predicted the evolution of host traits in response to parasitism. The coevolution of host and parasite life-history traits remains largely unexplored. We present an epidemiological model, based on resource allocation theory, that provides an analysis of the coevolution between host reproductive effort and parasite virulence. This model allows for hosts with either a fixed (i.e., genetic) or conditional (i.e., a phenotypically plastic) response to parasitism. It also considers superinfections. We show that parasitism always favors increased allocation to host reproduction, but because of epidemiological feedbacks, the evolutionarily stable host reproductive effort does not always increase with parasite virulence. Superinfection drives the evolution of parasite virulence and acts on the evolution of the host through parasite evolution, generally leading to higher host reproductive effort. Coevolution, as opposed to cases where only one of the antagonists evolves, may generate correlations between host and parasite life-history traits across environmental gradients affecting the fecundity or the survival of the host. Our results provide a theoretical framework against which experimental coevolution outcomes or field observations can be contrasted.     

THE GENETIC ARCHITECTURE OF PLASTICITY TO DENSITY IN IMPATIENS CAPENSIS

Plant responses to crowding may be mediated by resource availability and/or by a specific environmental cue, the ratio of red:far red wavelengths (R:FR) perceived by phytochrome. This study examined the contribution of phytochrome-mediated photomorphogenesis to genetic variation in plastic responses to density in the annual plant Impatiens capensis. Inbred lines derived from open and woodland populations were grown under low density high density, and high density with selective removal of FR wavelengths to block phytochrome-mediated perception of neighbor proximity. Genetic variation in plasticity to density and to the R:FR cue was detected for several traits Plants grown at high density displayed increased internode elongation; decreased branch, flower, and node production; increased menstem dormancy; and decreased leaf area and specific leaf weight compared to plants grown at low density. Stem elongation responses to density were suppressed when phytochrome perception was blocked at high density. For these phytochrome-mediated traits, a genotype's plasticity to density was strongly correlated with its response to R:FR. Phytochrome-mediated traits were tightly correlated with one another, regardless of the density environment. However, the responses to density of meristem allocation to branching and leaf traits were less strongly phytochrome-mediated. These traits differed in patterns of plasticity, and their genetic correlations often differed across environments. In particular, genetic trade-offs involving meristem allocation to branching were expressed only at low density. The observed density dependence of phenotypic and genetic correlations implies that indirect selection and the potential for correlated response to selection will depend upon the competitive environment. Thus the differential sensitivity of characters to the R:FR cue can influence the evolution of integrated plastic responses to density.     

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.     

Tradeoff between physical and chemical defense in plant seeds is mediated by seed mass

Plants have evolved both physical and chemical defenses to make the nutrients of attacked organs difficult to access or more toxic to resist animal consumption or/and pathogen attack. Although it is intuitive that a tradeoff could exist between physical and chemical defenses because of finite defense resources, many studies have failed to detect this tradeoff. We hypothesized that tradeoff between physical and chemical defenses in individual organs was mediated by the total resource allocation to those organs. In this study, we tested whether a tradeoff between physical (i.e. fiber content, which has proved to be a good indicator of investment into seed coat) and chemical defenses (i.e. total phenolics, which are abundant chemical defenses in plant seeds) existed in plant seeds by using 163 common species collected from Xishuangbanna tropical forest, southwest China. Then we tested whether this tradeoff was mediated by seed mass which could be a potential proxy of total resource investment per seed. Among the 163 species, there was large interspecific variation in both total phenolics (from 0.01 to 20.52%) and fiber content (from 4.47 to 81.49%). Our results supported our hypothesis: negative relationships between physical and chemical defenses were much stronger among small seeds than among large seeds. Our study suggests that total resource acquisition must be considered when evaluating defense tradeoffs. However, it is usually extremely difficult to measure this resource acquisition variation, thus we suggest utilizing easily measured proxies of acquisition variation to quantify tradeoffs.     

Constancy of the G matrix in ecological time

The constancy of the genetic variance-covariance matrix (G matrix) across environments and populations has been discussed and tested empirically over the years but no consensus has so far been reached. In this paper, I present a model in which morphological traits develop hierarchically, and individuals differ in their resource allocation and acquisition patterns. If the variance in resource acquisition is many times larger than the variance in resource allocation then strong genetic correlations are expected, and with almost isometric relations among traits. As the variation in resource acquisition decreases below a certain threshold, the correlations decrease overall and the relations among traits become a function of the allocation patterns, and in particular reflecting the basal division of allocation. A strong bottleneck can break a pattern of strong genetic correlation, but this effect diminishes rapidly with increasing bottleneck size. This model helps to understand why some populations change their genetic correlations in different environments, whereas others do not, since the key factor is the relation between the variances in resource acquisition and allocation. If a change in environment does not lead to a change in this ratio, no change can be expected, whereas if the ratio is changed substantially then major changes can be expected. This model can also help to understand the constancy of morphological patterns within larger taxa as a function of constancy in resource acquisition patterns over time and environments. When this pattern breaks, for example on islands, larger changes can be expected.     

Allocation tradeoffs and life histories: a conceptual and graphical framework

Tradeoffs – negative reciprocal causal relationships in net benefits between trait magnitudes – have not always been studied in depth appropriate to their central role in life‐history analysis. Here we focus on allocation tradeoffs, in which acquisition of a limiting resource requires allocation of resource to alternative traits. We identify the components of this allocation process and emphasize the importance of quantifying them. We then propose categorizing allocation tradeoffs into linear, concave and convex relationships based on the way that resource allocation yields trait magnitudes under the tradeoff. Linear relationships are over‐represented in the literature because of typically small data sets over restricted ranges of trait magnitudes, an emphasis on simple correlation analysis, and a failure to remove variation associated with acquisition of the limiting resource in characterizing the tradeoff. (We provide methods for controlling these acquisition effects.) Non‐linear relationships have been documented and are expected under plausible conditions that we summarize. We note ways that shifting environments and biological features yield plasticity of tradeoff graphs. Finally, we illustrate these points using case studies and close with priorities for future work.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

How is life history variation generated from the genetic resource allocation?

A simple quantitative genetic model is proposed to explain the observed genetic correlation structure of a bruchid beetleCallosobruchus chinensis in terms of two underlying variables: the resource acquisition and the resource allocation. Heritabilities and genetic correlations among age-specific, fecundities are regarded as consequences of genetic variations of the two variables. Genetic correlations are predominantly positive in both predictions and observations. Nonetheless, comparison between observed and predicted values in heritabilities, genetic correlations, and genetic principal components suggested significant genetic variances both of the resource allocation and the resource acquisition. The prediction of the model is discussed in relation, to experimental tests of trade-off in life history evolution.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.     

Phenotypic and Genetic Effects of Contrasting Ethanol Environments on Physiological and Developmental Traits in Drosophila melanogaster

A central problem in evolutionary physiology is to understand the relationship between energy metabolism and fitness-related traits. Most attempts to do so have been based on phenotypic correlations that are not informative for the evolutionary potential of natural populations. Here, we explored the effect of contrasting ethanol environments on physiological and developmental traits, their genetic (co)variances and genetic architecture in Drosophila melanogaster. Phenotypic and genetic parameters were estimated in two populations (San Fernando and Valdivia, Chile), using a half-sib family design where broods were split into ethanol-free and ethanol-supplemented conditions. Our findings show that metabolic rate, body mass and development times were sensitive (i.e., phenotypic plasticity) to ethanol conditions and dependent on population origin. Significant heritabilities were found for all traits, while significant genetic correlations were only found between larval and total development time and between development time and metabolic rate for flies of the San Fernando population developed in ethanol-free conditions. Posterior analyses indicated that the G matrices differed between ethanol conditions for the San Fernando population (mainly explained by differences in genetic (co)variances of developmental traits), whereas the Valdivia population exhibited similar G matrices between ethanol conditions. Our findings suggest that ethanol-free environment increases the energy available to reduce development time. Therefore, our results indicate that environmental ethanol could modify the process of energy allocation, which could have consequences on the evolutionary response of natural populations of D. melanogaster.     

The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust?

Plant populations and species differ greatly in phenotypic plasticity. This could be because plasticity is advantageous under some conditions and disadvantageous or not advantageous under others. We distinguish adaptive from injurious and neutral plasticity and discuss when selection should favor adaptive plasticity over genetic differentiation or lack of phenotypic variation. It seems reasonable to hypothesize that selection is likely to favor plasticity when an environmental factor varies on the same spatial scale as the plant response unit, when the plant can respond to an environmental factor faster than the level of the factor changes, and when environmental variation is highly but not completely predictable. Phenotypic plasticity might also tend to be more advantageous when mean resource availability is high rather than low, when a response can occur late in development rather than early, and when a response is reversible rather than irreversible. There is substantial evidence for the hypothesis that predictability favors plasticity. However, available evidence does not support the hypothesis that high mean resource availability necessarily favors plasticity. Testing hypotheses about when it is good for a plant to adjust is central to understanding the diversity of plasticity in plants.     

Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness?

Understanding the factors that constrain the reproductive success of animals and their demographics requires detailed insight into the processes of resource acquisition and allocation in relation to habitat richness. Parasitoid wasp females are valuable models in this respect because their lifetime reproductive success is closely tied to host availability. Parasitoids that manufacture eggs throughout adult life (i.e. ‘synovigenic’ species) and characteristically acquire nutrients via feeding are predicted to be plastic in their allocation to egg manufacture. Using the synovigenic parasitoid wasp Venturia canescens, we tested whether this prediction holds when females are faced with variation in the availability of both hosts and food. Laboratory experiments were conducted to determine how environmental variation affects parasitoid reproductive success and the lifetime dynamics of egg load and of major nutrient types. Our results, surprisingly, show that female V. canescens lacks a significant degree of reproductive plasticity under our experimental conditions. In particular, allocation of resources to reproduction was high irrespective of host availability. We attribute this lack of flexibility to the low energy content of V. canescens' eggs and to features peculiar to the ecology of this species. Our findings shed new light on the physiological factors that constrain parasitoid lifetime reproductive success. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 621–632.     

Plasticity of seed output in response to soil nutrients and density in Abutilon theophrasti: implications for maintenance of genetic variation

 Seed output is determined by two processes: resource acquisition and the allocation of resources to seeds. In order to clarify how the reaction norm of seed output is controlled by the phenotypic expression of its two components, we examined the genetic components of plasticity of seed dry mass, plant size, and reproductive allocation under different conditions of soil nutrient availability and conspecific competition among eight families of Abutilon theophrasti. Without competition, the reaction norm of seed mass of the families crossed between the lowest and other nutrient levels, although neither of its components, plant size and reproductive allocation, showed such a response. The crossing reaction norm (i.e., reversal of relative fitnesses of different genotypes along the environmental gradient) of seed mass resulted from (1) a trade-off between plant size and reproductive allocation, and (2) changes in the relative magnitude of genetic variances in plant size and reproductive allocation with soil nutrient availability. While allocation was more important in determining seed mass under limiting nutrient conditions, plant size became more important under high-nutrient conditions. There were no significant genetic variances in seed mass, plant size, and reproductive allocation in the competition treatment, except at the highest nutrient level. The results show that plant competition mitigated the effects of genetic differences in plant performance among the families. We discuss the results in relation to maintenance of genetic variation within a population. Received: 16 August 1996 / Accepted 26 April 1997