Genetic variance in fitness and its cross-sex covariance predict adaptation during experimental evolution

The additive genetic variation (V_A) of fitness in a population is of particular importance to quantify its adaptive potential and predict its response to rapid environmental change. Recent statistical advances in quantitative genetics and the use of new molecular tools have fostered great interest in estimating fitness V_A in wild populations. However, the value of V_A for fitness in predicting evolutionary changes over several generations remains mostly unknown. In our study, we addressed this question by combining classical quantitative genetics with experimental evolution in the model organism Tribolium castaneum (red flour beetle) in three new environmental conditions (Dry, Hot, Hot-Dry). We tested for potential constraints that might limit adaptation, including environmental and sex genetic antagonisms captured by negative genetic covariance between environments and female and male fitness, respectively. Observed fitness changes after 20 generations mainly matched our predictions. Given that body size is commonly used as a proxy for fitness, we also tested how this trait and its genetic variance (including nonadditive genetic variance) were impacted by environmental stress. In both traits, genetic variances were sex and condition dependent, but they differed in their variance composition, cross-sex and cross-environment genetic covariances, as well as in the environmental impact on V_A.     

Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness

Ecological conditions affect fitness, but mechanisms causing such effects are not well known, while evolved responses to environmental variation may depend on the underlying mechanisms. Consequences of environmental conditions vary strongly between traits, but a framework to interpret such variation is lacking. We propose that variation in trait response may be explained by differential canalisation, with traits with larger fitness effects showing weaker responses to environmental perturbations due to preferential resource allocation to such traits. We tested the canalisation hypothesis using brood size manipulation in wild jackdaw nestlings in which we measured eight physiological traits (mainly oxidative stress markers), and two feather traits. For each trait, we estimated manipulation response and association with fitness (over‐winter survival). As predicted, a strong negative correlation emerged between manipulation response and association with fitness (r =?0.76). We discuss the consequences of differential trait canalisation for the study of mechanisms mediating environmental effects on fitness.     

Adaptation in the face of internal conflict: the paradox of the organism revisited

The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within-organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi-level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness-maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.     

Evidence of developmental niche construction in dung beetles: effects on growth,scaling and reproductive success

Niche construction occurs when organisms modify their environments and alter selective conditions through their physiology and behaviours. Such modifications can bias phenotypic variation and enhance organism–environment fit. Yet few studies exist that experimentally assess the degree to which environmental modifications shape developmental and fitness outcomes, how their influences may differ among species and identify the underlying proximate mechanisms. Here, we experimentally eliminate environmental modifications from the developmental environment of Onthophagus dung beetles. We show that these modifications (1) differentially influence growth among species, (2) consistently shape scaling relationships in fitness‐related traits, (3) are necessary for the maintenance of sexual dimorphism, (4) influence reproductive success among females of at least one species and (5) implicate larval cultivation of an external rumen as a possible mechanism for environmental modification. Our results present evidence that Onthophagus larvae engage in niche construction, and that this is a fundamental component of beetle development and fitness.     

Brain plasticity over the metamorphic boundary: carry-over effect of larval environment on froglet brain development

Brain development shows high plasticity in response to environmental heterogeneity. However, it is unknown how environmental variation during development may affect brain architecture across life history switch points in species with complex life cycles. Previously, we showed that predation and competition affect brain development in common frog (Rana temporaria) tadpoles. Here, we studied whether larval environment had carry-over effects in brains of metamorphs. Tadpoles grown at high density had large optic tecta at metamorphosis, whereas tadpoles grown under predation risk had small diencephala. We found that larval density had a carry-over effect on froglet optic tectum size, whereas the effect of larval predation risk had vanished by metamorphosis. We discuss the possibility that the observed changes may be adaptive, reflecting the needs of an organism in given environmental and developmental contexts.     

Manipulating the strength of organism–environment feedback increases nonlinearity and apparent hysteresis of ecosystem response to environmental change

Theory predicts that organism–environment feedbacks play a central role in how ecological communities respond to environmental change. Strong feedback causes greater nonlinearity between environmental change and ecosystem state, increases the likelihood of hysteresis in response to environmental change, and augments the possibility of alternative stable regimes. To illustrate these predictions and their dependence on a temporal scale, we simulated a minimal ecosystem model. To test the predictions, we manipulated the feedback strength between the metabolism and the dissolved oxygen concentration in an aquatic heterotrophic tri‐trophic community in microecosystems. The manipulation consisted of five levels, ranging from low to high feedback strength by altering the oxygen diffusivity: free gas exchange between the microcosm atmosphere and the external air (metabolism not strongly affecting environmental oxygen), with the regular addition of 200, 100, or 50 ml of air and no gas exchange. To test for nonlinearity and hysteresis in response to environmental change, all microecosystems experienced a gradual temperature increase from 15 to 25°C and then back to 15°C. We regularly measured the dissolved oxygen concentration, total biomass, and species abundance. Nonlinearity and hysteresis were higher in treatments with stronger organism–environment feedbacks. There was no evidence that stronger feedback increased the number of observed ecosystem states. These empirical results are in broad agreement with the theory that stronger feedback increases nonlinearity and hysteresis. They therefore represent one of the first direct empirical tests of the importance of feedback strength. However, we discuss several limitations of the study, which weaken confidence in this interpretation. Research demonstrating the causal effects of feedback strength on ecosystem responses to environmental change should be placed at the core of efforts to plan for sustainable ecosystems.     

Tracking unstable states: ecosystem dynamics in a changing world

Ecological systems can show complex and sometimes abrupt responses to environmental change, with important implications for their resilience. Theories of alternate stable states have been used to predict regime shifts of ecosystems as equilibrium responses to sufficiently slow environmental change. The actual rate of environmental change is a key factor affecting the response, yet we are still lacking a non-equilibrium theory that explicitly considers the influence of this rate of environmental change. We present a metacommunity model of predator–prey interactions displaying multiple stable states, and we impose an explicit rate of environmental change in habitat quality (carrying capacity) and connectivity (dispersal rate). We study how regime shifts depend on the rate of environmental change and compare the outcome with a stability analysis in the corresponding constant environment. Our results reveal that in a changing environment, the community can track states that are unstable in the constant environment. This tracking can lead to regime shifts, including local extinctions, that are not predicted by alternative stable state theory. In our metacommunity, tracking unstable states also controls the maintenance of spatial heterogeneity and spatial synchrony. Tracking unstable states can also lead to regime shifts that may be reversible or irreversible. Our study extends current regime shift theories to integrate rate-dependent responses to environmental change. It reveals the key role of unstable states for predicting transient dynamics and long-term resilience of ecological systems to climate change.     

Ecological immunology in a fluctuating environment: an integrative analysis of tree swallow nestling immune defense

Evolutionary ecologists have long been interested by the link between different immune defenses and fitness. Given the importance of a proper immune defense for survival, it is important to understand how its numerous components are affected by environmental heterogeneity. Previous studies targeting this question have rarely considered more than two immune markers. In this study, we measured seven immune markers (response to phytohemagglutinin (PHA), hemolysis capacity, hemagglutination capacity, plasma bactericidal capacity, percentage of lymphocytes, percentage of heterophils, and percentage of eosinophils) in tree swallow (Tachycineta bicolor) nestlings raised in two types of agro‐ecosystems of contrasted quality and over 2 years. First, we assessed the effect of environmental heterogeneity (spatial and temporal) on the strength and direction of correlations between immune measures. Second, we investigated the effect of an immune score integrating information from several immune markers on individual performance (including growth, mass at fledging and parasite burden). Both a multivariate and a pair‐wise approach showed variation in relationships between immune measures across years and habitats. We also found a weak association between the integrated score of nestling immune function and individual performance, but only under certain environmental conditions. We conclude that the ecological context can strongly affect the interpretation of immune defenses in the wild. Given that spatiotemporal variations are likely to affect individual immune defenses, great caution should be used when generalizing conclusions to other study systems.     

Tipping points in tropical tree cover: linking theory to data

It has recently been found that the frequency distribution of remotely sensed tree cover in the tropics has three distinct modes, which seem to correspond to forest, savanna, and treeless states. This pattern has been suggested to imply that these states represent alternative attractors, and that the response of these systems to climate change would be characterized by critical transitions and hysteresis. Here, we show how this inference is contingent upon mechanisms at play. We present a simple dynamical model that can generate three alternative tree cover states (forest, savanna, and a treeless state), based on known mechanisms, and use this model to simulate patterns of tree cover under different scenarios. We use these synthetic data to show that the hysteresis inferred from remotely sensed tree cover patterns will be inflated by spatial heterogeneity of environmental conditions. On the other hand, we show that the hysteresis inferred from satellite data may actually underestimate real hysteresis in response to climate change if there exists a positive feedback between regional tree cover and precipitation. Our results also indicate that such positive feedback between vegetation and climate should cause direct shifts between forest and a treeless state (rather than through an intermediate savanna state) to become more likely. Finally, we show how directionality of historical change in conditions may bias the observed relationship between tree cover and environmental conditions.     

Looking for a needle in a haystack: inference about individual fitness components in a heterogeneous population

Studies of wild vertebrates have provided evidence of substantial differences in lifetime reproduction among individuals and the sequences of life history ‘states’ during life (breeding, nonbreeding, etc.). Such differences may reflect ‘fixed’ differences in fitness components among individuals determined before, or at the onset of reproductive life. Many retrospective life history studies have translated this idea by assuming a ‘latent’ unobserved heterogeneity resulting in a fixed hierarchy among individuals in fitness components. Alternatively, fixed differences among individuals are not necessarily needed to account for observed levels of individual heterogeneity in life histories. Individuals with identical fitness traits may stochastically experience different outcomes for breeding and survival through life that lead to a diversity of ‘state’ sequences with some individuals living longer and being more productive than others, by chance alone. The question is whether individuals differ in their underlying fitness components in ways that cannot be explained by observable ‘states’ such as age, previous breeding success, etc. Here, we compare statistical models that represent these opposing hypotheses, and mixtures of them, using data from kittiwakes. We constructed models that accounted for observed covariates, individual random effects (unobserved heterogeneity), first‐order Markovian transitions between observed states, or combinations of these features. We show that individual sequences of states are better accounted for by models incorporating unobserved heterogeneity than by models including first‐order Markov processes alone, or a combination of both. If we had not considered individual heterogeneity, models including Markovian transitions would have been the best performing ones. We also show that inference about age‐related changes in fitness components is sensitive to incorporation of underlying individual heterogeneity in models. Our approach provides insight into the sources of individual heterogeneity in life histories, and can be applied to other data sets to examine the ubiquity of our results across the tree of life.     

Environmental variation alters the fitness effects of rifampicin resistance mutations in Pseudomonas aeruginosa

The fitness effects of antibiotic resistance mutations in antibiotic‐free conditions play a key role in determining the long‐term maintenance of resistance. Although resistance is usually associated with a cost, the impact of environmental variation on the cost of resistance is poorly understood. Here, we test the impact of heterogeneity in temperature and resource availability on the fitness effects of antibiotic resistance using strains of the pathogenic bacterium Pseudomonas aeruginosa carrying clinically important rifampicin resistance mutations. Although the rank order of fitness was generally maintained across environments, fitness effects relative to the wild type differed significantly. Changes in temperature had a profound impact on the fitness effects of resistance, whereas changes in carbon substrate had only a weak impact. This suggests that environmental heterogeneity may influence whether the costs of resistance are likely to be ameliorated by second‐site compensatory mutations or by reversion to wild‐type rpoB. Our results highlight the need to consider environmental heterogeneity and genotype‐by‐environment interactions for fitness in models of resistance evolution.     

Does Dormancy Increase Fitness of Bacterial Populations in Time-Varying Environments?

A simple family of models of a bacterial population in a time varying environment in which cells can transit between dormant and active states is constructed. It consists of a linear system of ordinary differential equations for active and dormant cells with time-dependent coefficients reflecting an environment which may be periodic or random, with alternate periods of low and high resource levels. The focus is on computing/estimating the dominant Lyapunov exponent, the fitness, and determining its dependence on various parameters and the two strategies—responsive and stochastic—by which organisms switch between dormant and active states. A responsive switcher responds to good and bad times by making timely and appropriate transitions while a stochastic switcher switches continuously without regard to the environmental state. The fitness of a responsive switcher is examined and compared with fitness of a stochastic switcher, and with the fitness of a dormancy-incapable organism. Analytical methods show that both switching strategists have higher fitness than a dormancy-incapable organism when good times are rare and that responsive switcher has higher fitness than stochastic switcher when good times are either rare or common. Numerical calculations show that stochastic switcher can be most fit when good times are neither too rare or too common. This research was supported by NSF Grant DMS 0414270, Department of Mathematics, Arizona State University, Tempe, AZ.     

CHARACTERIZING SELECTION ON PHENOTYPIC PLASTICITY IN RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal‐scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full‐sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full‐sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes.     

Multivariate selection shapes environment-dependent variation in the clonal morphology of a red seaweed

Within-individual strategies of variation (e.g., phenotypic plasticity) are particularly relevant to modular organisms, in which ramets of the same genetic individual may encounter diverse environments imposing diverse patterns of selection. Hence, measuring selection in heterogeneous environments is essential to understanding whether environment-dependent phenotypic change enhances the fitness of modular individuals. In sublittoral marine habitats, competition for light and space among modular taxa generates extreme patchiness in resource availability. Little is known, however, of the potential for plasticity within individuals to arise from spatially-variable selection in such systems. We tested whether plasticity enhances genet-level fitness in Asparagopsis armata, a clonal seaweed in which correlated traits mediate morphological responses to variation in light. Using the capacity for rapid, clonal growth to measure fitness, we identified aspects of ramet morphology targeted by selection in two contrasting light environments and compared patterns of selection across environments. We found that directional selection on single traits, coupled with linear and nonlinear selection on multi-trait interactions, shape ramet morphology within environments and favor different phenotypes in each. Evidence of environment-dependent, multivariate selection on correlated traits is novel for any marine modular organism and demonstrates that seaweeds, such as A. armata, may potentially adapt to environmental heterogeneity via plasticity in clonal morphology.     

Nutrient control of neural stem cells

The physiological status of an organism is able to influence stem cell behaviour to ensure that stem cells meet the needs of the organism during growth, and in response to injury and environmental changes. In particular, the brain is sensitive to metabolic fluctuations. Here we discuss how nutritional status is able to regulate systemic and local insulin/IGF signalling so as to control aspects of neural stem behaviour. Recent results have begun to reveal how systemic signals are relayed to neural stem cells through local interactions with a glial niche. Although much still remains to be discovered, emerging parallels between the regulation of Drosophila and mammalian stem cells suggest a conserved mechanism for how the brain responds to changes in nutritional state.     

Specific proteomic adaptation to distinct environments in Vibrio parahaemolyticus includes significant fluctuations in expression of essential proteins

Bacteria constantly experience changes to their external milieu and need to adapt accordingly to ensure their survival. Certain bacteria adapt by means of cellular differentiation, resulting in the development of a specific cell type that is specialized for life in a distinct environment. Furthermore, to understand how bacteria adapt, it is essential to appreciate the significant changes that occur at the proteomic level. By analysing the proteome of our model organism Vibrio parahaemolyticus from distinct environmental conditions and cellular differential states, we demonstrate that the proteomic expression profile is highly flexible, which likely allows it to adapt to life in different environmental conditions and habitats. We show that, even within the same swarm colony, there are specific zones of cells with distinct expression profiles. Furthermore, our data indicate that cell surface attachment and swarmer cell differentiation are distinct programmes that require specific proteomic expression profiles. This likely allows V. parahaemolyticus to adapt to life in different environmental conditions and habitats. Finally, our analyses reveal that the expression profile of the essential protein pool is highly fluid, with significant fluctuations that dependent on the specific life-style, environment and differentiation state of the bacterium.     

The selective advantage of reaction norms for environmental tolerance

A tolerance curve defines the dependence of a genotype's fitness on the state of an environmental gradient. It can be characterized by a mode (the genotype's optimal environment) and a width (the breadth of adaptation). It seems possible that one or both of these characters can be modified in an adaptive manner, at least partially, during development. Thus, we extend the theory of environmental tolerance to include reaction norms for the mode and the width of the tolerance curve. We demonstrate that the selective value of such reaction norms increases with increasing spatial heterogeneity and between-generation temporal variation in the environment and with decreasing within-generation temporal variation. Assuming that the maintenance of a high breadth of adaptation is costly, reaction, norms are shown to induce correlated selection for a reduction in this character. Nevertheless, regardless of the magnitude of the reaction norm, there is a nearly one to one relationship between the optimal breadth of adaptation and the within-generation temporal variation perceived by the organism. This suggests that empirical estimates of the breadth of adaptation may provide a useful index of this type of environmental variation from the organism's point of view.     

舍曲林对蚤状溞诱导型反捕食防御代内与代际可塑性的干扰效应

表型可塑性是指生物(尤其是单一基因型)在适应异质环境时表达出不同表型的能力,并且有遗传基础。环境变化调控表型可塑性既可以发生在个体发育进程中(称为代内表型可塑性),也能够以可遗传表型响应的形式持续多个生物世代(称为代际表型可塑性)。浮游动物枝角类常常受到来自鱼类的捕食风险影响而表现出诱导型防御的表型可塑性。诱导型防御的表达在很大程度上受到代谢稳态控制,因此枝角类的诱导型防御的表达容易受到内稳态代谢干扰物(例如抗抑郁药舍曲林)的影响。考虑到舍曲林在水中生物活性高且难以被降解;同时,枝角类世代周期较短,因此需要评估连续多代舍曲林暴露对枝角类反捕食防御代内以及代际可塑性的影响。结果发现：在代内可塑性方面,连续两代的舍曲林暴露放大了鱼类信息素诱导的蚤状溞体长减小趋势以及相对尾刺长度增长趋势,但是对鱼类信息素作用下的种群适合度参数无明显干扰。在代际可塑性方面,随着连续两代舍曲林的浓度上升,亲代经历鱼类信息素产下的子代继续响应鱼类信息素时,体长减小、相对尾刺长度增大,说明形态防御得到加强;同时种群净繁殖量以及种群内禀增长率下降的趋势被放大,由此可能抑制鱼类捕食风险下蚤状溞的种群丰度。上述结果表明,...     

Metabolomics and its role in understanding cellular responses in plants

A natural shift is taking place in the approaches being adopted by plant scientists in response to the accessibility of systems-based technology platforms. Metabolomics is one such field, which involves a comprehensive non-biased analysis of metabolites in a given cell at a specific time. This review briefly introduces the emerging field and a range of analytical techniques that are most useful in metabolomics when combined with computational approaches in data analyses. Using cases from Arabidopsis and other selected plant systems, this review highlights how information can be integrated from metabolomics and other functional genomics platforms to obtain a global picture of plant cellular responses. We discuss how metabolomics is enabling large-scale and parallel interrogation of cell states under different stages of development and defined environmental conditions to uncover novel interactions among various pathways. Finally, we discuss selected applications of metabolomics. This special review article is dedicated to the commemoration of the retirement of Dr. Oluf L. Gamborg after 25 years of service as Founding Managing Editor of Plant Cell Reports. RB and KN have contributed equally to this review.