Perspective: Intransitive Eco-Evolutionary Feedback Loops Maintain Coexistence

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.

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.

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.

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.

A stabilizing eco-evolutionary feedback loop in the wild

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.

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.

Studies have shown the potential for rapid adaptation in coevolving populations and that the structure of species interaction networks can modulate the vulnerability of ecological systems to perturbations. Although the feedback loop between population dynamics and coevolution of traits is crucial for understanding long-term stability in ecological assemblages, modelling eco-evolutionary dynamics in species-rich assemblages is still a challenge. We explore how eco-evolutionary feedbacks influence trait evolution and species abundances in 23 empirical antagonistic networks. We show that, if selection due to antagonistic interactions is stronger than other selective pressures, eco-evolutionary feedbacks lead to higher mean species abundances and lower temporal variation in abundances. By contrast, strong selection of antagonistic interactions leads to higher temporal variation of traits and on interaction strengths. Our results present a theoretical link between the study of the species persistence and coevolution in networks of interacting species, pointing out the ways by which coevolution may decrease the vulnerability of species within antagonistic networks to demographic fluctuation.

The idea that ecology and evolution can influence each other simultaneously in a feedback loop has become the lynchpin of the new field of eco-evolutionary dynamics (Pelletier et al. 2009). However, under a different name, eco-evolutionary dynamics is actually a venerable idea. Biologists, starting with Darwin (1859) and later Brown and Wilson (1956), have long recognized that competitive interactions between species lead to evolutionary divergence that facilitates coexistence, an eco-evolutionary process known as character displacement. Despite all the attention lavished on eco-evolutionary feedbacks in recent years, character displacement is often neglected. This neglect likely reflects an uneasy combination of over-familiarity (hasn’t it all been done many times over?) and a lingering skepticism after rancorous debates over ecological character displacement and reinforcement. With renewed interest in eco-evolutionary feedbacks, it is time for a synthetic review to resuscitate the original eco-evolutionary process. Pfennig and Pfennig (2012), who have produced a series of elegant touchstone studies on both ecological and reproductive character displacement in spadefoot toads (Spea), are ideally qualified to write such a review. With Evolution’s Wedge: Competition and the Origins of Diversity (2012), they have succeeded. The book posits that competition is a ubiquitous ecological process and that competition’s consequence, character displacement, is an evolutionary wedge that generates biodiversity. Pfennig and Pfennig argue that this wedge provides a unifying theory for fundamental questions throughout evolutionary biology and ecology. In the first chapter, Pfennig and Pfennig cover the basics: definitions, alternative outcomes, and criteria for demonstrating character displacement. The subsequent three chapters provide thorough, and at times speculative, discussions of why, when, and how character displacement occurs. Although each section addresses reproductive and ecological character displacement separately, Pfennig and Pfennig also provide insightful discussions of how the two types of character displacement facilitate and impede evolution of the other. The second half of the book examines how character displacement influences other ecological and evolutionary patterns and processes, like the formation of intraspecies diversity, niche formation, community composition, sexual selection, speciation, and macroevolution. Pfennig and Pfennig bring valuable perspective to aspects of character displacement that are usually overlooked. For example, they argue that phenotypic plasticity is a key component of character displacement. Plasticity can reveal cryptic genetic variation and consequently may delay competitive exclusion long enough for genetically canalized differences to evolve. Moreover, variation in plasticity itself can be heritable, and thus the strength of plasticity can evolve during character displacement. In addition, the authors attempt to dissolve the dichotomy between reproductive character displacement and reinforcement. Finally, the book includes many examples from the plant literature, something rarely done in the discussion of character displacement. Evolution’s Wedge is not an exhaustive summary of all relevant examples of each phenomenon discussed. Instead, Pfennig and Pfennig focus on historically important and iconic empirical examples with helpful diagrams to cover the essential concepts. The authors seem to have made a conscious decision not to discuss the extensive theoretical research on character displacement in detail. They often refer to general conclusions derived from mathematical models, but never discuss the mathematical details. Some readers may find the lack of equations inviting in a book primarily concerned with general concepts, whereas others may see this as an unfortunate missed opportunity to define and discuss

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.

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'.

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.

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.

Microbial communities abound with examples of complex social interactions that shape microbial ecosystems. One particularly striking example is microbial cooperation via the secretion of public goods. It has been suggested by theory, and recently demonstrated experimentally, that microbial population dynamics and the evolutionary dynamics of cooperative social genes take place with similar timescales, and are linked to each other via an eco-evolutionary feedback loop. We overview this recent evidence, and discuss the possibility that a third process may be also part of this loop: phenotypic dynamics. Complex social strategies may be implemented at the single-cell level by means of gene regulatory networks. Thus gene expression plasticity or stochastic gene expression, both of which may occur with a timescale of one to a few generations, can potentially lead to a three-way coupling between behavioral dynamics, population dynamics, and evolutionary dynamics

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.