Eco-evolutionary Feedback Loop Research Articles

Ongoing convergent evolution of a selfing syndrome threatens plant-pollinator interactions.

Plant-pollinator interactions evolved early in the angiosperm radiation. Ongoing environmental changes are however leading to pollinator declines that may cause pollen limitation to plants and change the evolutionary pressures shaping plant mating systems. We used resurrection ecology methodology to contrast ancestors and contemporary descendants in four natural populations of the field pansy (Viola arvensis) in the Paris region (France), a depauperate pollinator environment. We combine population genetics analysis, phenotypic measurements and behavioural tests on a common garden experiment. Population genetics analysis reveals 27% increase in realized selfing rates in the field during this period. We documented trait evolution towards smaller and less conspicuous corollas, reduced nectar production and reduced attractiveness to bumblebees, with these trait shifts convergent across the four studied populations. We demonstrate the rapid evolution of a selfing syndrome in the four studied plant populations, associated with a weakening of the interactions with pollinators over the last three decades. This study demonstrates that plant mating systems can evolve rapidly in natural populations in the face of ongoing environmental changes. The rapid evolution towards a selfing syndrome may in turn further accelerate pollinator declines, in an eco-evolutionary feedback loop with broader implications to natural ecosystems.

Experimentally simulating the evolution-to-ecology connection: Divergent predator morphologies alter natural food webs

The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite-that adaptive evolution alters ecological processes-has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard (Anolis sagrei). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop.

Importance of interindividual interactions in eco-evolutionary population dynamics: The rise of demo-genetic agent-based models.

The study of eco-evolutionary dynamics, that is of the intertwinning between ecological and evolutionary processes when they occur at comparable time scales, is of growing interest in the current context of global change. However, many eco-evolutionary studies overlook the role of interindividual interactions, which are hard to predict and yet central to selective values. Here, we aimed at putting forward models that simulate interindividual interactions in an eco-evolutionary framework: the demo-genetic agent-based models (DG-ABMs). Being demo-genetic, DG-ABMs consider the feedback loop between ecological and evolutionary processes. Being agent-based, DG-ABMs follow populations of interacting individuals with sets of traits that vary among the individuals. We argue that the ability of DG-ABMs to take into account the genetic heterogeneity-that affects individual decisions/traits related to local and instantaneous conditions-differentiates them from analytical models, another type of model largely used by evolutionary biologists to investigate eco-evolutionary feedback loops. Based on the review of studies employing DG-ABMs and explicitly or implicitly accounting for competitive, cooperative or reproductive interactions, we illustrate that DG-ABMs are particularly relevant for the exploration of fundamental, yet pressing, questions in evolutionary ecology across various levels of organization. By jointly modelling the effects of management practices and other eco-evolutionary processes on interindividual interactions and population dynamics, DG-ABMs are also effective prospective and decision support tools to evaluate the short- and long-term evolutionary costs and benefits of management strategies and to assess potential trade-offs. Finally, we provide a list of the recent practical advances of the ABM community that should facilitate the development of DG-ABMs.

Eco-evolutionary dynamics of bimatrix games

Feedbacks between strategies and the environment are common in social-ecological, evolutionary ecological and even psychological-economic systems. Using common resources is always a dilemma for community members, like the tragedy of the commons. Here, we consider replicator dynamics with feedback-evolving games, where the pay-offs switch between two different matrices. Although each pay-off matrix on its own represents an environment where cooperators and defectors cannot coexist stably, we show that it is possible to design appropriate switching control laws and achieve persistent oscillations of strategy abundance. This result should help guide the widespread problem of population state control in microbial experiments and other social problems with eco-evolutionary feedback loops.

Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework

I provide a general framework for linking ecology and evolution. I start from the fact that individuals require energy, trace molecules, water, and mates to survive and reproduce, and that phenotypic resource accrual traits determine an individual9s ability to detect and acquire these resources. Optimum resource accrual traits, and their values, are determined by the dynamics of resources, aspects of the environment that hinder resource detection and acquisition by imposing risks of mortality and reproductive failure, and the energetic costs of developing and maintaining the traits -- part of an individual9s energy budget. These budgets also describe how individuals utilize energy by partitioning it into maintenance, development and/or reproduction at each age and size, age and size at sexual maturity, and the size and number of offspring produced at each reproductive event. The optimum energy budget is consequently determined by the optimum life history strategy that describes how resources are utilized to maximize fitness by trading off investments in maintenance, development, and reproductive output at each age and size. The optimum life history in turn determines body size. An eco-evolutionary feedback loop occurs when resource accrual traits evolve to impact the quality and quantity of resources that individuals accrue, resulting in a new optimum life history strategy and energy budget required to deliver it, a change in body size, and altered population dynamics that, in turn, impact the resource base. These feedback loops can be complex, but can be studied by examining the eco-evolutionary journey of communities from one equilibrium state to another following a perturbation to the environment.

Size‐dependent eco‐evolutionary feedbacks in harvested systems

Harvesting may drive body downsizing along with population declines and decreased harvesting yields. These changes are commonly construed as consequences of direct harvest selection, where small‐bodied, early‐reproducing individuals are immediately favoured. However, together with directly selecting against a large body size, harvesting and body downsizing alter many ecological features, such as competitive and trophic interactions, and thus also indirectly reshape natural selection acting back on body sizes through eco‐evolutionary feedback loops (EEFLs). We sketch plausible scenarios of simple EEFLs in which one‐dimensional, density‐dependent natural selection acts either antagonistically or synergistically with direct harvest selection on body size. Antagonistic feedbacks favour body‐size stasis but erode genetic variability and associated body‐size evolvability, and may ultimately impair population persistence and recovery. In contrast, synergistic feedbacks drive fast evolution towards smaller body sizes and favour population resilience, but may have far‐reaching bottom–up or top–down effects. We illustrate the further complexities resulting from multiple environmental feedbacks using a co‐evolving predator–prey pair, in which case outcomes from EEFLs depend not only on population densities, but also on whether prey sit above or below the optimal predator/prey body‐size ratio, and whether prey are more or less evolvable than their predators. EEFLs improve our ability to understand and predict nature's response to harvesting, but their integration into the research agenda will require a full consideration of the effects and dynamics of natural selection.

Eco-Evolutionary Feedbacks and the Maintenance of Metacommunity Diversity in a Changing Environment.

The presence and strength of resource competition can influence how organisms adaptively respond to environmental change. Selection may thus reflect a balance between two forces, adaptation to an environmental optimum and evolution to avoid strong competition. While this phenomenon has previously been explored in the context of single communities, its implications for eco-evolutionary dynamics at the metacommunity scale are largely unknown. We developed a simulation model for the evolution of a quantitative trait that influences both an organism’s carrying capacity and its intra- and interspecific competitive ability. In the model, multiple species inhabit a three-patch landscape, and we investigated the effect of varying the connectivity level among patches, the presence and pace of directional environmental change, and the strength of competition between the species. Our model produced some patterns previously observed in evolving metacommunity models, such as species sorting and community monopolization. However, we found that species sorting was diminished even at low rates of dispersal and was influenced by competition strength, and that monopolization was observed only when environmental change was very rapid. We also detected an eco-evolutionary feedback loop between local phenotypic evolution at one site and competition at another site, which maintains species diversity in some conditions. The existence of a feedback loop maintained by dispersal indicates that eco-evolutionary dynamics in communities operate at a landscape scale.

The eco-evolutionary dynamics of a predator-prey system across an r/K continuum

The effects of a single trait on more than one ecological function is called ecological pleiotropy. Traits that exhibit ecological pleiotropy are relevant to eco-evolutionary dynamics because the structure of interaction between the trait and its ecological functions alters how eco-evolutionary feedback loops emerge. Density-dependent selection (DDS) assumes that a single trait affects both density-independent and density-dependent population growth through ecological pleiotropy, and is one of the simplest routes for feedback loops. The r/K theory proposes a mechanism by which DDS occurs, but its predictions were poorly explored in an eco-evolutionary context. Some assumptions of the r/K theory seems to be relevant for the eco-evolution of predator-prey interactions. However, the relationship between these theories were poorly explored. Here, we investigate how does the r/K theory relates to the eco-evolution of predator-prey systems. We seek to answer two questions: (1) What are the system’s parameters that affect the predominance of r- and K-selection? (2) Does system’s qualitative behaviour depends on whether the predominant selection on prey population is an r- or a K-selection? To answer these questions, we built a model of differential equations describing the eco-evolutionary dynamics of a predator-prey system. We assume that prey vulnerability to predation is an adaptive trait that affects preys density-dependent growth rate through ecological pleiotropy. Then, we partitioned the selection gradient in its r- and K-selection components and evaluate how their magnitude relates to systems behaviour. We found that stable predator-prey cycles only occurs when K-selection is predominant. When r-selection is predominant, cycles lead to a runaway dynamics. Furthermore, the way predators parameters affect prey position in the r/K continuum depends on how they affect predation risk. While increasing predation risk increases K-selection, decreasing it increases r-selection. We discuss the relevance of the structure of ecological pleiotropy to our results and the perspectives that unifies the r/K theory and eco-evolutionary dynamics.

Ecological and Evolutionary Processes Shaping Viral Genetic Diversity.

The contemporary genomic diversity of viruses is a result of the continuous and dynamic interaction of past ecological and evolutionary processes. Thus, genome sequences of viruses can be a valuable source of information about these processes. In this review, we first describe the relevant processes shaping viral genomic variation, with a focus on the role of host–virus coevolution and its potential to give rise to eco-evolutionary feedback loops. We further give a brief overview of available methodology designed to extract information about these processes from genomic data. Short generation times and small genomes make viruses ideal model systems to study the joint effect of complex coevolutionary and eco-evolutionary interactions on genetic evolution. This complexity, together with the diverse array of lifetime and reproductive strategies in viruses ask for extensions of existing inference methods, for example by integrating multiple information sources. Such integration can broaden the applicability of genetic inference methods and thus further improve our understanding of the role viruses play in biological communities.

Theoretical Approaches in Evolutionary Ecology: Environmental Feedback as a Unifying Perspective.

Evolutionary biology and ecology have a strong theoretical underpinning, and this has fostered a variety of modeling approaches. A major challenge of this theoretical work has been to unravel the tangled feedback loop between ecology and evolution. This has prompted the development of two main classes of models. While quantitative genetics models jointly consider the ecological and evolutionary dynamics of a focal population, a separation of timescales between ecology and evolution is assumed by evolutionary game theory, adaptive dynamics, and inclusive fitness theory. As a result, theoretical evolutionary ecology tends to be divided among different schools of thought, with different toolboxes and motivations. My aim in this synthesis is to highlight the connections between these different approaches and clarify the current state of theory in evolutionary ecology. Central to this approach is to make explicit the dependence on environmental dynamics of the population and evolutionary dynamics, thereby materializing the eco-evolutionary feedback loop. This perspective sheds light on the interplay between environmental feedback and the timescales of ecological and evolutionary processes. I conclude by discussing some potential extensions and challenges to our current theoretical understanding of eco-evolutionary dynamics.

Antibiotic resistance in the wild: an eco-evolutionary perspective.

The legacy of the use and misuse of antibiotics in recent decades has left us with a global public health crisis: antibiotic-resistant bacteria are on the rise, making it harder to treat infections. At the same time, evolution of antibiotic resistance is probably the best-documented case of contemporary evolution. To date, research on antibiotic resistance has largely ignored the complexity of interactions that bacteria engage in. However, in natural populations, bacteria interact with other species; for example, competition and grazing are import interactions influencing bacterial population dynamics. Furthermore, antibiotic leakage to natural environments can radically alter bacterial communities. Overall, we argue that eco-evolutionary feedback loops in microbial communities can be modified by residual antibiotics and evolution of antibiotic resistance. The aim of this review is to connect some of the well-established key concepts in evolutionary biology and recent advances in the study of eco-evolutionary dynamics to research on antibiotic resistance. We also identify some key knowledge gaps related to eco-evolutionary dynamics of antibiotic resistance, and review some of the recent technical advantages in molecular microbiology that offer new opportunities for tackling these questions. Finally, we argue that using the full potential of evolutionary theory and active communication across the different fields is needed for solving this global crisis more efficiently.This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences'.

Body size, not maladaptive gene flow, explains death-feigning behaviour in Timema cristinae stick insects

Eco-evolutionary feedback loops, where rapid evolution influences the ecology of an organism and subsequently alters the evolutionary trajectory of the population, are intriguing possibilities, but evidence for or against them is scarce. Timema cristinae stick insects express variation within and among populations in the expression of death-feigning behaviour, but the causes of variation in this species is not known. Here, I test the hypothesis that variation in death feigning across populations stems from an eco-evolutionary feedback loop, whereby gene flow causes poor camouflage, which increases the strength of bird predation, and ultimately drives the evolution of increased death-feigning. By conducting behavioural trials on eight T. cristinae populations that differ in the degree of maladaptive gene flow incurred, I falsify the eco-evolutionary feedback hypothesis for the evolution of death-feigning. Instead, I show that smaller individuals are more likely to feign death than larger individuals. By rearing individuals in the lab, I offer suggestive evidence that the body size effect is explained by the age of wild-caught individuals: younger individuals feign death more than older individuals. These findings add an example to the literature where no eco-evolutionary feedback exists in a system for which other similar feedbacks have been found, and provide evidence that death-feigning behaviour depends on body size.

Cry-wolf signals emerging from coevolutionary feedbacks in a tritrophic system.

For a communication system to be stable, senders should convey honest information. Providing dishonest information, however, can be advantageous to senders, which imposes a constraint on the evolution of communication systems. Beyond single populations and bitrophic systems, one may ask whether stable communication systems can evolve in multitrophic systems. Consider cross-species signalling where herbivore-induced plant volatiles (HIPVs) attract predators to reduce the damage from arthropod herbivores. Such plant signals may be honest and help predators to identify profitable prey/plant types via HIPV composition and to assess prey density via the amount of HIPVs. There could be selection for dishonest signals that attract predators for protection from possible future herbivory. Recently, we described a case in which plants release a fixed, high amount of HIPVs independent of herbivore load, adopting what we labelled a 'cry-wolf' strategy. To understand when such signals evolve, we model coevolutionary interactions between plants, herbivores and predators, and show that both 'honest' and 'cry-wolf' types can emerge, depending on the assumed plant-herbivore encounter rates and herbivore population density. It is suggested that the 'cry-wolf' strategy may have evolved to reduce the risk of heavy damage in the future. Our model suggests that eco-evolutionary feedback loops involving a third species may have important consequences for the stability of this outcome.

Eco-evolutionary dynamics: investigating multiple causal pathways linking changes in behavior, population density and natural selection

Correlations between population density, natural selection and phenotypic change are widespread and may comprise an eco-evolutionary feedback loop, yet we still know very little about the causes of connections between them. Isolating the mechanistic links in eco-evolutionary feedback loops, both in terms of identifying sources of variation in traits and in terms of determining how and why natural selection varies with population density, can provide key insight into avian population dynamics. Here, we summarize more than a decade of findings in western bluebirds (Sialia mexicana) to illustrate the multiple and potentially interacting mechanisms that can cause simultaneous changes in traits and population density. In previous work, we discovered correlated changes in aggression, population density and natural selection during the process of colonization. Here we provide evidence that density-dependent selection, maternal effects and demographic consequences of selection on aggression may all play a role in driving feedback between phenotypic change and population density. Thus, this system provides an example of the multiple mechanistic links that can produce such feedback loops and emphasizes the importance of investigating alternative hypotheses for correlated patterns of ecological and phenotypic change even when there is strong evidence that natural selection is acting on a trait. Ultimately, identifying these mechanisms is crucial, as eco-evolutionary feedback have the potential to explain avian population cycles, range dynamics, population persistence, and even patterns of species coexistence.

Stochastic dynamics of adaptive trait and neutral marker driven by eco-evolutionary feedbacks.

How the neutral diversity is affected by selection and adaptation is investigated in an eco-evolutionary framework. In our model, we study a finite population in continuous time, where each individual is characterized by a trait under selection and a completely linked neutral marker. Population dynamics are driven by births and deaths, mutations at birth, and competition between individuals. Trait values influence ecological processes (demographic events, competition), and competition generates selection on trait variation, thus closing the eco-evolutionary feedback loop. The demographic effects of the trait are also expected to influence the generation and maintenance of neutral variation. We consider a large population limit with rare mutation, under the assumption that the neutral marker mutates faster than the trait under selection. We prove the convergence of the stochastic individual-based process to a new measure-valued diffusive process with jumps that we call Substitution Fleming-Viot Process (SFVP). When restricted to the trait space this process is the Trait Substitution Sequence first introduced by Metz et al. (1996). During the invasion of a favorable mutation, a genetical bottleneck occurs and the marker associated with this favorable mutant is hitchhiked. By rigorously analysing the hitchhiking effect and how the neutral diversity is restored afterwards, we obtain the condition for a time-scale separation; under this condition, we show that the marker distribution is approximated by a Fleming-Viot distribution between two trait substitutions. We discuss the implications of the SFVP for our understanding of the dynamics of neutral variation under eco-evolutionary feedbacks and illustrate the main phenomena with simulations. Our results highlight the joint importance of mutations, ecological parameters, and trait values in the restoration of neutral diversity after a selective sweep.

Density-dependent selection closes an eco-evolutionary feedback loop in the stick insect Timema cristinae.

Empirical demonstrations of feedbacks between ecology and evolution are rare. Here, we used a field experiment to test the hypothesis that avian predators impose density-dependent selection (DDS) on Timema cristinae stick insects. We transplanted wild-caught T. cristinae to wild bushes at 50 : 50 cryptic : conspicuous morph ratio and manipulated density by transplanting either 24 or 48 individuals. The frequency of the conspicuous morph was reduced by 73% in the low-density treatment, but only by 50% in the high-density treatment, supporting a hypothesis of negative DDS. Coupled with previous studies on T. cristinae, which demonstrate that maladaptive gene flow reduces population density, we support an eco-evolutionary feedback loop in this system. Furthermore, our results support the hypothesis that predator satiation is the mechanism driving DDS. We found no effects of T. cristinae density on the abundance or species richness of other arthropods. Eco-evolutionary feedbacks, driven by processes like DDS, can have implications for adaptive divergence and speciation.

Feedback between Population and Evolutionary Dynamics Determines the Fate of Social Microbial Populations

Author SummaryThe fact that rapid evolution within a species can cause dramatic ecological changes has only recently begun to be appreciated. In particular, it has often been assumed that population dynamics, controlled by ecological circumstances such as the presence of predators or disease, occur at such different timescales compared with evolutionary dynamics that they are effectively de-coupled. Recent studies, however, have found that evolution can occur over ecological timescales and thus may have important effects on ecological dynamics. Here, we demonstrate the presence of a tight coupling between population dynamics and the evolutionary dynamics of a “social” microbial gene, which allows a laboratory population of budding yeast to cooperatively break down sucrose and grow on the simpler sugars released from it. In such cooperative populations, evolution may favor non-cooperative, or “cheater” individuals that do not contribute to the public good (in this case, the products of sucrose break down), but still use that public good to grow at the expense of the individuals that do cooperate. Our study shows that a population of cooperators that is invaded by cheaters does not collapse as a result of cheater proliferation but can evolve to a viable equilibrium. However, the coexisting population is less resilient to perturbations.

Experimental Test of an Eco-Evolutionary Dynamic Feedback Loop between Evolution and Population Density in the Green Peach Aphid

An eco-evolutionary feedback loop is defined as the reciprocal impacts of ecology on evolutionary dynamics and evolution on ecological dynamics on contemporary timescales. We experimentally tested for an eco-evolutionary feedback loop in the green peach aphid, Myzus persicae, by manipulating initial densities and evolution. We found strong evidence that initial aphid density alters the rate and direction of evolution, as measured by changes in genotype frequencies through time. We also found that evolution of aphids within only 16 days, or approximately three generations, alters the rate of population growth and predicts density compared to nonevolving controls. The impact of evolution on population dynamics also depended on density. In one evolution treatment, evolution accelerated population growth by up to 10.3% at high initial density or reduced it by up to 6.4% at low initial density. The impact of evolution on population growth was as strong as or stronger than that caused by a threefold change in intraspecific density. We found that, taken together, ecological condition, here intraspecific density, alters evolutionary dynamics, which in turn alter concurrent population growth rate (ecological dynamics) in an eco-evolutionary feedback loop. Our results suggest that ignoring evolution in studies predicting population dynamics might lead us to over- or underestimate population density and that we cannot predict the evolutionary outcome within aphid populations without considering population size.

The functional genomics of an eco‐evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics

Feedbacks between ecological and evolutionary change may play important roles in community and ecosystem functioning, but a complete eco-evolutionary feedback loop has not been demonstrated at the community level, and we know little about molecular mechanisms underlying this kind of eco-evolutionary dynamics. In predator-prey (rotifer-alga) microcosms, cyclical changes in predator abundance generated fluctuating selection for a heritable prey defence trait, cell clumping. Predator population growth was affected more by prey evolution than by changes in prey abundance, and changes in predator abundance drove further prey evolution, completing the feedback loop. Within a predator-prey cycle, genes up-regulated as clumping declined were down-regulated as clumping increased, and vice-versa. Genes changing most in expression tended to be associated with defence or its cost. Expression patterns of individual genes differed greatly between consecutive cycles (often reversing direction), suggesting that a particular phenotype may be produced by several (perhaps many) different gene transcription pathways.

Intense or Spatially Heterogeneous Predation Can Select against Prey Dispersal

Dispersal theory generally predicts kin competition, inbreeding, and temporal variation in habitat quality should select for dispersal, whereas spatial variation in habitat quality should select against dispersal. The effect of predation on the evolution of dispersal is currently not well-known: because predation can be variable in both space and time, it is not clear whether or when predation will promote dispersal within prey. Moreover, the evolution of prey dispersal affects strongly the encounter rate of predator and prey individuals, which greatly determines the ecological dynamics, and in turn changes the selection pressures for prey dispersal, in an eco-evolutionary feedback loop. When taken all together the effect of predation on prey dispersal is rather difficult to predict. We analyze a spatially explicit, individual-based predator-prey model and its mathematical approximation to investigate the evolution of prey dispersal. Competition and predation depend on local, rather than landscape-scale densities, and the spatial pattern of predation corresponds well to that of predators using restricted home ranges (e.g. central-place foragers). Analyses show the balance between the level of competition and predation pressure an individual is expected to experience determines whether prey should disperse or stay close to their parents and siblings, and more predation selects for less prey dispersal. Predators with smaller home ranges also select for less prey dispersal; more prey dispersal is favoured if predators have large home ranges, are very mobile, and/or are evenly distributed across the landscape.