Genetic evolution,plasticity, and bet‐hedging as adaptive responses to temporally autocorrelated fluctuating selection: A quantitative genetic model

Adaptive responses to autocorrelated environmental fluctuations through evolution in mean reaction norm elevation and slope and an independent component of the phenotypic variance are analyzed using a quantitative genetic model. Analytic approximations expressing the mutual dependencies between all three response modes are derived and solved for the joint evolutionary outcome. Both genetic evolution in reaction norm elevation and plasticity are favored by slow temporal fluctuations, with plasticity, in the absence of microenvironmental variability, being the dominant evolutionary outcome for reasonable parameter values. For fast fluctuations, tracking of the optimal phenotype through genetic evolution and plasticity is limited. If residual fluctuations in the optimal phenotype are large and stabilizing selection is strong, selection then acts to increase the phenotypic variance (bet‐hedging adaptive). Otherwise, canalizing selection occurs. If the phenotypic variance increases with plasticity through the effect of microenvironmental variability, this shifts the joint evolutionary balance away from plasticity in favor of genetic evolution. If microenvironmental deviations experienced by each individual at the time of development and selection are correlated, however, more plasticity evolves. The adaptive significance of evolutionary fluctuations in plasticity and the phenotypic variance, transient evolution, and the validity of the analytic approximations are investigated using simulations.     

Life‐history evolution under fluctuating density‐dependent selection and the adaptive alignment of pace‐of‐life syndromes

We present a novel perspective on life‐history evolution that combines recent theoretical advances in fluctuating density‐dependent selection with the notion of pace‐of‐life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short‐lived, bold, aggressive and highly dispersive ‘fast’ types at one end of the POLS to the less fecund, long‐lived, cautious, shy, plastic and socially responsive ‘slow’ types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco‐evolutionary dynamics with population density – a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density‐dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density‐dependent selection. Phenotypic plasticity and/or genetic (co‐)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density‐dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life‐history evolution and thus our ability to predict natural population dynamics.     

The distribution of fitness effects in an uncertain world

The distribution of fitness effects (DFE) among new mutations plays a critical role in adaptive evolution and the maintenance of genetic variation. Although fitness landscape models predict several key features of the DFE, most theory to date focuses on predictable environmental conditions, while ignoring stochastic environmental fluctuations that feature prominently in the ecology of many organisms. Here, we derive an extension of Fisher's geometric model that incorporates two common effects of environmental variation: (1) nonadaptive genotype‐by‐environment interactions (G × E), in which the phenotype of a given genotype varies across environmental contexts; and (2) random fluctuation of the fitness optimum, which generates fluctuating selection. We show that both factors cause a mismatch between the DFE within single generations and the distribution of geometric mean fitness effects (averaged over multiple generations) that governs long‐term evolutionary change. Such mismatches permit strong evolutionary constraints—despite an abundance of beneficial fitness variation within single environmental contexts—and to conflicting DFE estimates from direct versus indirect inference methods. Finally, our results suggest an intriguing parallel between the genetics and ecology of evolutionary constraints, with environmental fluctuations and pleiotropy placing qualitatively similar limits on the availability of adaptive genetic variation.     

Isolation by distance,not incipient ecological speciation,explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis,Line‐cheeked Spinetail) despite near threefold body size change across an environmental gradient

During the process of ecological speciation, reproductive isolation results from divergent natural selection and leads to a positive correlation between genetic divergence and adaptive phenotypic divergence, that is, isolation by adaptation (IBA). In natural populations, phenotypic differentiation is often autocorrelated with geographic distance, making IBA difficult to distinguish from the neutral expectation of isolation by distance (IBD). We examined these two alternatives in a dramatic case of clinal phenotypic variation in an Andean songbird, the Line‐cheeked Spinetail (Cranioleuca antisiensis). At its geographic extremes, this species shows a near threefold difference in body mass (11.5 to 31.0 g) with marked plumage differences. We analysed phenotypic, environmental and genetic data (5,154 SNPs) from 172 individuals and 19 populations sampled along its linear distribution in the Andes. We found that body mass was tightly correlated with environmental temperature, consistent with local adaptation as per Bergmann's rule. Using a P_ST–F_ST analysis, we found additional support for natural selection driving body mass differentiation, but these results could also be explained by environment‐mediated phenotypic plasticity. When we assessed the relative support for patterns of IBA and IBD using variance partitioning, we found that IBD was the best explanation for genetic differentiation along the cline. Adaptive phenotypic or environmental divergence can reduce gene flow, a pattern interpreted as evidence of ecological speciation's role in diversification. Our results provide a counterexample to this interpretation. Despite conditions conducive to ecological speciation, our results suggest that dramatic size and environmental differentiation within C. antisiensis are not limiting gene flow.     

The fitness threshold model: Random environmental change alters adaptive landscapes

We used a probabilistic optimization model to explore the joint evolutionary effects of random phenotypic and environmental variation. Two forms of environmental noise were defined in which the optimal phenotype remained constant but all organisms experienced either the same proportionate or the same absolute fitness gains and losses. There was no evolutionary effect of proportionate fitness fluctuations. In contrast, the optimal genotype varied with absolute fitness fluctuations, despite the environmental effect being phenotype-independent. We refer to such phenotype-independent fluctuation in absolute fitness as the fitness threshold model, because shared fitness effects determine the zero-fitness points (i.e. the baseline) on an intrinsic fitness function. Thus, environmental effects that are unrelated to a focal trait can cause peak shifts in the genetic optimum for the trait. Changes in the fitness threshold not only changed peak locations, but also altered the slopes defining the peaks, and so should alter the rate of evolution towards optima. This model pertains to evolution in any system, unless there is no phenotypic or environmental variance, or the selection function and distribution of phenotypic error assume similar shapes. Our results have many basic and applied implications for topics such as the maintenance of genetic variation, the canalization of development and the management of natural populations.     

Fluctuating selection and its (elusive) evolutionary consequences in a wild rodent population

Temporal fluctuations in the strength and direction of selection are often proposed as a mechanism that slows down evolution, both over geological and contemporary timescales. Both the prevalence of fluctuating selection and its relevance for evolutionary dynamics remain poorly understood however, especially on contemporary timescales: unbiased empirical estimates of variation in selection are scarce, and the question of how much of the variation in selection translates into variation in genetic change has largely been ignored. Using long‐term individual‐based data for a wild rodent population, we quantify the magnitude of fluctuating selection on body size. Subsequently, we estimate the evolutionary dynamics of size and test for a link between fluctuating selection and evolution. We show that, over the past 11 years, phenotypic selection on body size has fluctuated significantly. However, the strength and direction of genetic change have remained largely constant over the study period; that is, the rate of genetic change was similar in years where selection favoured heavier vs. lighter individuals. This result suggests that over shorter timescales, fluctuating selection does not necessarily translate into fluctuating evolution. Importantly however, individual‐based simulations show that the correlation between fluctuating selection and fluctuating evolution can be obscured by the effect of drift, and that substantially more data are required for a precise and accurate estimate of this correlation. We identify new challenges in measuring the coupling between selection and evolution, and provide methods and guidelines to overcome them.     

Hot spots become cold spots: coevolution in variable temperature environments

Antagonistic coevolution between hosts and parasites is a key process in the genesis and maintenance of biological diversity. Whereas coevolutionary dynamics show distinct patterns under favourable environmental conditions, the effects of more realistic, variable conditions are largely unknown. We investigated the impact of a fluctuating environment on antagonistic coevolution in experimental microcosms of Pseudomonas fluorescens SBW25 and lytic phage SBWΦ2. High‐frequency temperature fluctuations caused no deviations from typical coevolutionary arms race dynamics. However, coevolution was stalled during periods of high temperature under intermediate‐ and low‐frequency fluctuations, generating temporary coevolutionary cold spots. Temperature variation affected population density, providing evidence that eco‐evolutionary feedbacks act through variable bacteria–phage encounter rates. Our study shows that environmental fluctuations can drive antagonistic species interactions into and out of coevolutionary cold and hot spots. Whether coevolution persists or stalls depends on the frequency of change and the environmental optima of both interacting players.     

Environmentally‐induced noise dampens and reddens with increasing trophic level in a complex food web

Stochastic variability of key abiotic factors including temperature, precipitation and the availability of light and nutrients greatly influences species’ ecological function and evolutionary fate. Despite such influence, ecologists have typically ignored the effect of abiotic stochasticity on the structure and dynamics of ecological networks. Here we help to fill that gap by advancing the theory of how abiotic stochasticity, in the form of environmental noise, affects the population dynamics of species within food webs. We do this by analysing an allometric trophic network model of Lake Constance subjected to positive (red), negative (blue), and non‐autocorrelated (white) abiotic temporal variability (noise) introduced into the carrying capacity of basal species. We found that, irrespective of the colour of the introduced noise, the temporal variability of the species biomass within the network both reddens (i.e. its positive autocorrelation increases) and dampens (i.e. the magnitude of variation decreases) as the environmental noise is propagated through the food web by its feeding interactions from the bottom to the top. The reddening reflects a buffering of the noise‐induced population variability by complex food web dynamics such that non‐autocorrelated oscillations of noise‐free deterministic dynamics become positively autocorrelated. Our research helps explain frequently observed red variability of natural populations by suggesting that ecological processing of environmental noise through food webs with a range of species’ body sizes reddens population variability in nature.     

QUANTIFYING EVOLUTIONARY POTENTIAL OF MARINE FISH LARVAE: HERITABILITY,SELECTION, AND EVOLUTIONARY CONSTRAINTS

For many marine fish, intense larval mortality may provide considerable opportunity for selection, yet much less is known about the evolutionary potential of larval traits. We combined field demographic studies and manipulative experiments to estimate quantitative genetic parameters for both larval size and swimming performance for a natural population of a common coral‐reef fish, the bicolor damselfish (Stegastes partitus). We also examined selection on larval size by synthesizing information from published estimates of selective mortality. We introduce a method that uses the Lande–Arnold framework for examining selection on quantitative traits to empirically reconstruct adaptive landscapes. This method allows the relationship between phenotypic value and fitness components to be described across a broad range of trait values. Our results suggested that despite strong viability selection for large larvae and moderate heritability (h²= 0.29), evolutionary responses of larvae would likely be balanced by reproductive selection favoring mothers that produce more, smaller offspring. Although long‐term evolutionary responses of larval traits may be constrained by size‐number trade‐offs, our results suggest that phenotypic variation in larval size may be an ecologically important source of variability in population dynamics through effects on larval survival and recruitment to benthic populations.     

Is there plasticity in developmental instability? The effect of daily thermal fluctuations in an ectotherm

Diversified bet‐hedging (DBH) by production of within‐genotype phenotypic variance may evolve to maximize fitness in stochastic environments. Bet‐hedging is generally associated with parental effects, but phenotypic variation may also develop throughout life via developmental instability (DI). This opens for the possibility of a within‐generation mechanism creating DBH during the lifetime of individuals. If so, DI could in fact be a plastic trait itself; if a fluctuating environment indicates uncertainty about future conditions, sensing such fluctuations could trigger DI as a DBH response. However, this possibility has received little empirical attention. Here, we test whether fluctuating environments may elicit such a response in the clonally reproducing crustacean Daphnia magna. Specifically, we exposed genetically identical individuals to two environments of different thermal stability (stable vs. pronounced daily realistic temperature fluctuations) and tested for effects on DI in body mass and metabolic rate shortly before maturation. Furthermore, we also estimated the genetic variation in DI. Interestingly, fluctuating temperatures did not affect body mass, but metabolic rate decreased. We found no evidence for plasticity in DI in response to environmental fluctuations. The lack of plasticity was common to all genotypes, and for both traits studied. However, we found considerable evolvability for DI, which implies a general evolutionary potential for DBH under selection for increased phenotypic variance.     

The role of environment and core‐margin effects on range‐wide phenotypic variation in a montane grasshopper

The integration of genetic information with ecological and phenotypic data constitutes an effective approach to gain insight into the mechanisms determining interpopulation variability and the evolutionary processes underlying local adaptation and incipient speciation. Here, we use the Pyrenean Morales grasshopper (Chorthippus saulcyi moralesi) as study system to (i) analyse the relative role of genetic drift and selection in range‐wide patterns of phenotypic differentiation and (ii) identify the potential selective agents (environment, elevation) responsible for variation. We also test the hypothesis that (iii) the development of dispersal‐related traits is associated with different parameters related to population persistence/turnover, including habitat suitability stability over the last 120 000 years, distance to the species distribution core and population genetic variability. Our results indicate that selection shaped phenotypic differentiation across all the studied morphological traits (body size, forewing length and shape). Subsequent analyses revealed that among‐population differentiation in forewing length was significantly explained by a temperature gradient, suggesting an adaptive response to thermoregulation or flight performance under contrasting temperature regimes. We found support for our hypothesis predicting a positive association between the distance to the species distribution core and the development of dispersal‐related morphology, which suggests an increased dispersal capability in populations located at range edges that, in turn, exhibit lower levels of genetic variability. Overall, our results indicate that range‐wide patterns of phenotypic variation are partially explained by adaptation in response to local environmental conditions and differences in habitat persistence between core and peripheral populations.     

Field heritability of a plant adaptation to fire in heterogeneous landscapes

The strong association observed between fire regimes and variation in plant adaptations to fire suggests a rapid response to fire as an agent of selection. It also suggests that fire‐related traits are heritable, a precondition for evolutionary change. One example is serotiny, the accumulation of seeds in unopened fruits or cones until the next fire, an important strategy for plant population persistence in fire‐prone ecosystems. Here, we evaluate the potential of this trait to respond to natural selection in its natural setting. For this, we use a SNP marker approach to estimate genetic variance and heritability of serotiny directly in the field for two Mediterranean pine species. Study populations were large and heterogeneous in climatic conditions and fire regime. We first estimated the realized relatedness among trees from genotypes, and then partitioned the phenotypic variance in serotiny using Bayesian animal models that incorporated environmental predictors. As expected, field heritability was smaller (around 0.10 for both species) than previous estimates under common garden conditions (0.20). An estimate on a subset of stands with more homogeneous environmental conditions was not different from that in the complete set of stands, suggesting that our models correctly captured the environmental variation at the spatial scale of the study. Our results highlight the importance of measuring quantitative genetic parameters in natural populations, where environmental heterogeneity is a critical aspect. The heritability of serotiny, although not high, combined with high phenotypic variance within populations, confirms the potential of this fire‐related trait for evolutionary change in the wild.     

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.     

Local adaptation,dispersal evolution,and the spatial eco‐evolutionary dynamics of invasion

Local adaptation and dispersal evolution are key evolutionary processes shaping the invasion dynamics of populations colonizing new environments. Yet their interaction is largely unresolved. Using a single‐species population model along a one‐dimensional environmental gradient, we show how local competition and dispersal jointly shape the eco‐evolutionary dynamics and speed of invasion. From a focal introduction site, the generic pattern predicted by our model features a temporal transition from wave‐like to pulsed invasion. Each regime is driven primarily by local adaptation, while the transition is caused by eco‐evolutionary feedbacks mediated by dispersal. The interaction range and cost of dispersal arise as key factors of the duration and speed of each phase. Our results demonstrate that spatial eco‐evolutionary feedbacks along environmental gradients can drive strong temporal variation in the rate and structure of population spread, and must be considered to better understand and forecast invasion rates and range dynamics.     

EVOLUTION OF PHENOTYPE–ENVIRONMENT ASSOCIATIONS BY GENETIC RESPONSES TO SELECTION AND PHENOTYPIC PLASTICITY IN A TEMPORALLY AUTOCORRELATED ENVIRONMENT

Covariation between population‐mean phenotypes and environmental variables, sometimes termed a “phenotype–environment association” (PEA), can result from phenotypic plasticity, genetic responses to natural selection, or both. PEAs can potentially provide information on the evolutionary dynamics of a particular set of populations, but this requires a full theoretical characterization of PEAs and their evolution. Here, we derive formulas for the expected PEA in a temporally fluctuating environment for a quantitative trait with a linear reaction norm. We compare several biologically relevant scenarios, including constant versus evolving plasticity, and the situation in which an environment affects both development and selection but at different time periods. We find that PEAs are determined not only by biological factors (e.g., magnitude of plasticity, genetic variation), but also environmental factors, such as the association between the environments of development and of selection, and in some cases the level of temporal autocorrelation. We also describe how a PEA can be used to estimate the relationship between an optimum phenotype and an environmental variable (i.e., the environmental sensitivity of selection), an important parameter for determining the extinction risk of populations experiencing environmental change. We illustrate this ability using published data on the predator‐induced morphological responses of tadpoles to predation risk.     

Species packing in eco‐evolutionary models of seasonally fluctuating environments

As ecology and evolution become ever more entwined, many areas of ecological theory are being re‐examined. Eco‐evolutionary analyses of classic coexistence mechanisms are yielding new insights into the structure and stability of communities. We examine fluctuation‐dependent coexistence models, identifying communities that are both ecologically and evolutionarily stable. Members of these communities possess distinct environmental preferences, revealing widespread patterns of limiting similarity. This regularity leads to consistent changes in the structure of communities across fluctuation regimes. However, at high amplitudes, subtle differences in the form of fluctuations dramatically affect the collapse of communities. We also show that identical fluctuations can support multiple evolutionarily stable communities – a novel example of alternative stable states within eco‐evolutionary systems. Consequently, the configuration of communities will depend on historical contingencies, including details of the adaptive process. Integrating evolution into the study of coexistence offers new insights, while enriching our understanding of ecology.     

Eco‐evolutionary feedback promotes Red Queen dynamics and selects for sex in predator populations

Although numerous hypotheses exist to explain the overwhelming presence of sexual reproduction across the tree of life, we still cannot explain its prevalence when considering all inherent costs involved. The Red Queen hypothesis states that sex is maintained because it can create novel genotypes with a selective advantage. This occurs when the interactions between species induce frequent environmental change. Here, we investigate whether coevolution and eco‐evolutionary feedback dynamics in a predator‐prey system allows for indirect selection and maintenance of sexual reproduction in the predator. Combining models and chemostat experiments of a rotifer‐algae system we show a continuous feedback between population and trait change along with recurrent shifts from selection by predation and competition for a limited resource. We found that a high propensity for sex was indirectly selected and was maintained in rotifer populations within environments containing these eco‐evolutionary dynamics; whereas within environments under constant conditions, predators evolved rapidly to lower levels of sex. Thus, our results indicate that the influence of eco‐evolutionary feedback dynamics on the overall evolutionary change has been underestimated.     

The temporal distribution of directional gradients under selection for an optimum

Temporal variation in phenotypic selection is often attributed to environmental change causing movements of the adaptive surface relating traits to fitness, but this connection is rarely established empirically. Fluctuating phenotypic selection can be measured by the variance and autocorrelation of directional selection gradients through time. However, the dynamics of these gradients depend not only on environmental changes altering the fitness surface, but also on evolution of the phenotypic distribution. Therefore, it is unclear to what extent variability in selection gradients can inform us about the underlying drivers of their fluctuations. To investigate this question, we derive the temporal distribution of directional gradients under selection for a phenotypic optimum that is either constant or fluctuates randomly in various ways in a finite population. Our analytical results, combined with population‐ and individual‐based simulations, show that although some characteristic patterns can be distinguished, very different types of change in the optimum (including a constant optimum) can generate similar temporal distributions of selection gradients, making it difficult to infer the processes underlying apparent fluctuating selection. Analyzing changes in phenotype distributions together with changes in selection gradients should prove more useful for inferring the mechanisms underlying estimated fluctuating selection.     

Testing the niche variation hypothesis with a measure of body condition

Individual variation and fitness are cornerstones of evolution by natural selection. The niche variation hypothesis (NVH) posits that when interspecific competition is relaxed, intraspecific competition should drive niche expansion by selection favoring use of novel resources and that among‐individual variation should confer a selective advantage. Population‐level niche expansion could be achieved by all individuals using all available resources, or by each individual using a unique combination of resources, thereby increasing among‐individual dietary niche variation. Although individual variation can lead to species‐level evolutionary and ecological change, observed variation does not ensure a beneficial outcome. We used carbon and nitrogen stable isotope analysis of claw keratin and a Bayesian stable isotope mixing model to estimate the summer (July–September) assimilated diet of individual female black Ursus americanus and brown U. arctos bears. We quantified variation in dietary niche in both populations, and assessed diet relative to percentage body fat. We hypothesized that if the NVH held, percentage body fat would be similar for individuals of the same species across much of the dietary range of observed proportional salmon contributions to individual bear diets. Although we found greater differences in dietary niches between than within species, we observed greater among‐individual dietary variation in the brown bear population. Moreover, we found that within each species individual female bears achieved similar ranges of percentage body fat at various levels of salmon in the diet. Our results provide support for the NVH. Linking individual dietary niches to measures of physiological condition related to fitness can offer new insights into eco‐evolutionary processes related to food resource use.     

Environmental correlates of geographic divergence in a phenotypic trait: A case study using bat echolocation

Divergence in phenotypic traits may arise from the interaction of different evolutionary forces, including different kinds of selection (e.g., ecological), genetic drift, and phenotypic plasticity. Sensory systems play an important role in survival and reproduction, and divergent selection on such systems may result in lineage diversification. Such diversification could be largely influenced by selection in different environments as a result of isolation by environment (IbE). We investigated this process using geographic variation in the resting echolocation frequency of the horseshoe bat species, Rhinolophus damarensis, as a test case. Bats were sampled along a latitudinal gradient ranging from 16°S to 32°S in the arid western half of southern Africa. We measured body size and peak resting frequencies (RF) from handheld individual bats. Three hypotheses for the divergence in RF were tested: (1) James’ Rule, (2) IbE, and (3) genetic drift through isolation by distance (IbD) to isolate the effects of body size, local climatic conditions, and geographic distance, respectively, on the resting frequency of R. damarensis. Our results did not support genetic drift because there was no correlation between RF variation and geographic distance. Our results also did not support James' Rule because there was no significant relationship between (1) geographic distances and RF, (2) body size and RF, or (3) body size and climatic variables. Instead, we found support for IbE in the form of a correlation between RF and both region and annual mean temperature, suggesting that RF variation may be the result of environmental discontinuities. The environmental discontinuities coincided with previously reported genetic divergence. Climatic gradients in conjunction with environmental discontinuities could lead to local adaptation in sensory signals and directed dispersal such that gene flow is restricted, allowing lineages to diverge. However, our study cannot exclude the role of processes like phenotypic plasticity in phenotypic variation.