Investigating the eco-evolutionary response of microbiomes to environmental change.

Microorganisms are the primary engines of biogeochemical processes and foundational to the provisioning of ecosystem services to human society. Free-living microbial communities (microbiomes) and their functioning are now known to be highly sensitive to environmental change. Given microorganisms' capacity for rapid evolution, evolutionary processes could play a role in this response. Currently, however, few models of biogeochemical processes explicitly consider how microbial evolution will affect biogeochemical responses to environmental change. Here, we propose a conceptual framework for explicitly integrating evolution into microbiome-functioning relationships. We consider how microbiomes respond simultaneously to environmental change via four interrelated processes that affect overall microbiome functioning (physiological acclimation, demography, dispersal and evolution). Recent evidence in both the laboratory and the field suggests that ecological and evolutionary dynamics occur simultaneously within microbiomes; however, the implications for biogeochemistry under environmental change will depend on the timescales over which these processes contribute to a microbiome's response. Over the long term, evolution may play an increasingly important role for microbially driven biogeochemical responses to environmental change, particularly to conditions without recent historical precedent.

SEED: A framework for integrating ecological stoichiometry and eco-evolutionary dynamics.

Characterising the extent and sources of intraspecific variation and their ecological consequences is a central challenge in the study of eco-evolutionary dynamics. Ecological stoichiometry, which uses elemental variation of organisms and their environment to understand ecosystem patterns and processes, can be a powerful framework for characterising eco-evolutionary dynamics. However, the current emphasis on the relative content of elements in the body (i.e. organismal stoichiometry) has constrained its application. Intraspecific variation in the rates at which elements are acquired, assimilated, allocated or lost is often greater than the variation in organismal stoichiometry. There is much to gain from studying these traits together as components of an 'elemental phenotype'. Furthermore, each of these traits can have distinct ecological effects that are underappreciated in the current literature. We propose a conceptual framework that explores how microevolutionary change in the elemental phenotype occurs, how its components interact with each other and with other traits, and how its changes can affect a wide range of ecological processes. We demonstrate how the framework can be used to generate novel hypotheses and outline pathways for future research that enhance our ability to explain, analyse and predict eco-evolutionary dynamics.

Behavioural differences underlie toxicity and predation variation in blooms of Prymnesium parvum.

Much of the evolutionary ecology of toxic algal blooms (TABs) remains unclear, including the role of algal toxins in the adaptive 'strategies' of TAB-forming species. Most eukaryotic TABs are caused by mixotrophs that augment autotrophy with organic nutrient sources, including competing algae (intraguild predation). We leverage the standing diversity of TABs formed by the toxic, invasive mixotroph Prymnesium parvum to identify cell-level behaviours involved in toxin-assisted predation using direct observations as well as comparisons between genetically distinct low- and high-toxicity isolates. Our results suggest that P. parvum toxins are primarily delivered at close range and promote subsequent prey capture/consumption. Surprisingly, we find opposite chemotactic preferences for organic (prey-derived) and inorganic nutrients between differentially toxic isolates, respectively, suggesting behavioural integration of toxicity and phagotrophy. Variation in toxicity may, therefore, reflect broader phenotypic integration of key traits that ultimately contribute to the remarkable flexibility, diversity, and success of invasive populations.

Eco-evolutionary maintenance of diversity in fluctuating environments.

Growing evidence suggests that temporally fluctuating environments are important in maintaining variation both within and between species. To date, however, studies of genetic variation within a population have been largely conducted by evolutionary biologists (particularly population geneticists), while population and community ecologists have concentrated more on diversity at the species level. Despite considerable conceptual overlap, the commonalities and differences of these two alternative paradigms have yet to come under close scrutiny. Here, we review theoretical and empirical studies in population genetics and community ecology focusing on the 'temporal storage effect' and synthesise theories of diversity maintenance across different levels of biological organisation. Drawing on Chesson's coexistence theory, we explain how temporally fluctuating environments promote the maintenance of genetic variation and species diversity. We propose a further synthesis of the two disciplines by comparing models employing traditional frequency-dependent dynamics and those adopting density-dependent dynamics. We then address how temporal fluctuations promote genetic and species diversity simultaneously via rapid evolution and eco-evolutionary dynamics. Comparing and synthesising ecological and evolutionary approaches will accelerate our understanding of diversity maintenance in nature.

"Resistance Is Futile": Weaker Selection for Resistance by Abundant Parasites Increases Prevalence and Depresses Host Density.

AbstractTheory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a "resistance is futile" outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts' resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, "transmission rate") along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations.

Taming fitness: Organism-environment interdependencies preclude long-term fitness forecasting.

Fitness is a central but notoriously vexing concept in evolutionary biology. The propensity interpretation of fitness is often regarded as the least problematic account for fitness. It ties an individual's fitness to a probabilistic capacity to produce offspring. Fitness has a clear causal role in evolutionary dynamics under this account. Nevertheless, the propensity interpretation faces its share of problems. We discuss three of these. We first show that a single scalar value is an incomplete summary of a propensity. Second, we argue that the widespread method of "abstracting away" environmental idiosyncrasies by averaging over reproductive output in different environments is not a valid approach when environmental changes are irreversible. Third, we point out that expanding the range of applicability for fitness measures by averaging over more environments or longer time scales (so as to ensure environmental reversibility) reduces one's ability to distinguish selectively relevant differences among individuals because of mutation and eco-evolutionary feedbacks. This series of problems leads us to conclude that a general value of fitness that is both explanatory and predictive cannot be attained. We advocate for the use of propensity-compatible methods, such as adaptive dynamics, which can accommodate these difficulties.

Integrating eco-evolutionary dynamics and modern coexistence theory.

Community ecology typically assumes that competitive exclusion and species coexistence are unaffected by evolution on the time scale of ecological dynamics. However, recent studies suggest that rapid evolution operating concurrently with competition may enable species coexistence. Such findings necessitate general theory that incorporates the coexistence contributions of eco-evolutionary processes in parallel with purely ecological mechanisms and provides metrics for quantifying the role of evolution in shaping competitive outcomes in both modelling and empirical contexts. To foster the development of such theory, here we extend the interpretation of the two principal metrics of modern coexistence theory-niche and competitive ability differences-to systems where competitors evolve. We define eco-evolutionary versions of these metrics by considering how invading and resident species adapt to conspecific and heterospecific competitors. We show that the eco-evolutionary niche and competitive ability differences are sums of ecological and evolutionary processes, and that they accurately predict the potential for stable coexistence in previous theoretical studies of eco-evolutionary dynamics. Finally, we show how this theory frames recent empirical assessments of rapid evolution effects on species coexistence, and how empirical work and theory on species coexistence and eco-evolutionary dynamics can be further integrated.

Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator.

Most research on eco-evolutionary feedbacks focuses on ecological consequences of evolution in a single species. This ignores the fact that evolution in response to a shared environmental factor in multiple species involved in interactions could alter the net cumulative effect of evolution on ecology. We empirically tested whether urbanization-driven evolution in a predator (nymphs of the damselfly Ischnura elegans) and its prey (the water flea Daphnia magna) jointly shape the outcome of predation under simulated heatwaves. Both interactors show genetic trait adaptation to urbanization, particularly to higher temperatures. We cross-exposed common-garden reared damselflies and Daphnia from replicated urban and rural populations, and quantified predation rates and functional response traits. Urban damselfly nymphs showed higher encounter and predation rates than rural damselflies when exposed to rural prey, but this difference disappeared when they preyed on urban Daphnia. This represents a case of a cryptic evo-to-eco feedback, where the evolution of one species dampens the effects of the evolution of another species on their interaction strength. The effects of evolution of each single species were strong: the scenario in which only the predator or prey was adapted to urbanization resulted in a c. 250% increase in encounter rate and a c. 25% increase in predation rate, compared to the rural predator-rural prey combination. Our results provide unique evidence for eco-evolutionary feedbacks in cities, and underscore the importance of a multi-species approach in eco-evolutionary dynamics research.

Cryptic eco-evolutionary feedback in the city.

Research Highlight: Brans, K. I., Tüzün, N., Sentis, A., De Meester, L., & Stoks, R. (2021). Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13601. Despite the strength and ubiquity of urban stressors on multiple taxa, there have been minimal attempts to determine the ecological consequences of urban evolution on multiple species. Brans & Tüzün et al. use a well-known predator prey system-damselfly nymphs Ischnura elegans and water fleas Daphnia magna-to test whether scenarios in which both species evolve in response to urbanization differ from scenarios in which only the predator or prey evolves. The authors show that urban damselflies showed higher encounter and predation rates when paired with rural prey, but that the advantages conferred by urbanization-driven adaptation disappeared when urban predators encountered urban prey. This represents a cryptic eco-evolutionary feedback, where evolution of both predator and prey concealed the effect of evolution in each partner individually. Results suggest that mismatches in the evolutionary responses of interacting species may have significant ecological consequences, and highlight the importance of a multi-species approach in eco-evolutionary dynamics research.

Towards a more precise - and accurate - view of eco-evolution.

Over the past 15 years, the number of papers focused on 'eco-evo dynamics' has increased exponentially (Figure 1). This pattern suggests the rapid growth of a new, integrative discipline. We argue this overstates the case. First, the terms 'eco-evo dynamics' and 'eco-evo interactions' are used too imprecisely. As a result, many studies that claim to describe eco-evo dynamics are actually describing basic ecological or evolutionary processes. Second, these terms are often used as if the study of how ecological and evolutionary processes are intertwined is novel when, in fact, it is not. The result is confusion over what the term 'eco-evolution' and its derivatives describe. We advocate a more precise definition of eco-evolution that is more useful in efforts to understand and characterise the diversity of ecological and evolutionary processes and that focuses attention on the subset of those processes that occur only when ecological and evolutionary timescales are comparable. [Figure: see text].

On the deformability of an empirical fitness landscape by microbial evolution.

A fitness landscape is a map between the genotype and its reproductive success in a given environment. The topography of fitness landscapes largely governs adaptive dynamics, constraining evolutionary trajectories and the predictability of evolution. Theory suggests that this topography can be deformed by mutations that produce substantial changes to the environment. Despite its importance, the deformability of fitness landscapes has not been systematically studied beyond abstract models, and little is known about its reach and consequences in empirical systems. Here we have systematically characterized the deformability of the genome-wide metabolic fitness landscape of the bacterium Escherichia coli Deformability is quantified by the noncommutativity of epistatic interactions, which we experimentally demonstrate in mutant strains on the path to an evolutionary innovation. Our analysis shows that the deformation of fitness landscapes by metabolic mutations rarely affects evolutionary trajectories in the short range. However, mutations with large environmental effects produce long-range landscape deformations in distant regions of the genotype space that affect the fitness of later descendants. Our results therefore suggest that, even in situations in which mutations have strong environmental effects, fitness landscapes may retain their power to forecast evolution over small mutational distances despite the potential attenuation of that power over longer evolutionary trajectories. Our methods and results provide an avenue for integrating adaptive and eco-evolutionary dynamics with complex genetics and genomics.

Phenotype-Environment Matching Predicts Both Positive and Negative Effects of Intraspecific Variation.

Natural populations can vary considerably in their genotypic and/or phenotypic diversity. Differences in this intraspecific diversity can have important consequences for contemporary ecological dynamics, but the direction and magnitude of these effects appear inconsistent across studies and systems. Here we proposed and tested the hypothesis that context-dependent ecological effects of altering phenotypic variance are predictable and arise from the relationship between a population's mean phenotype and the local environmental optimum. By factorially manipulating the mean and variance of a key host trait in environments with and without a lethal parasite, we demonstrate that increasing phenotypic variance can have beneficial effects for host populations (e.g., smaller disease epidemics) but only when the population's initial phenotype was poorly matched to the local environment. When phenotypes were initially well suited to environmental conditions, in contrast, greater phenotypic variance led to larger disease epidemics. Significant reductions in individual susceptibility occurred in both contexts over time, but the mechanisms leading to those reductions differed; strong selection was caused by either a suboptimal trait mean and insufficient trait variance or a near-optimal trait mean and too much trait variance. Increasing intraspecific variation is clearly not always beneficial for populations, instead producing predictable ecological and evolutionary effects that depend on environmental context and biological interactions.

Frequency of virus-resistant hosts determines experimental community dynamics.

Parasites, such as bacterial viruses (phages), can have large effects on host populations both at the ecological and evolutionary levels. In the case of cyanobacteria, phages can reduce primary production and infected hosts release intracellular nutrients influencing planktonic food web structure, community dynamics, and biogeochemical cycles. Cyanophages may be of great importance in aquatic food webs during large cyanobacterial blooms unless the host population becomes resistant to phage infection. The consequences on plankton community dynamics of the evolution of phage resistance in bloom forming cyanobacterial populations are still poorly studied. Here, we examined the effect of different frequencies of a phage-resistant genotype within a filamentous nitrogen-fixing Nodularia spumigena population on an experimental plankton community. Three Nodularia populations with different initial frequencies (0%, 5%, and 50%) of phage-resistant genotypes were inoculated in separate treatments with the phage 2AV2, the green alga Chlorella vulgaris, and the rotifer Brachionus plicatilis, which formed the experimental plankton community subjected to either nitrogen-limited or nitrogen-rich conditions. We found that the frequency of the phage-resistant Nodularia genotype determined experimental community dynamics. Cyanobacterial populations with a high frequency (50%) of the phage-resistant genotype dominated the cultures despite the presence of phages, retaining most of the intracellular nitrogen in the plankton community. In contrast, populations with low frequencies (0% and 5%) of the phage-resistant genotype were lysed and reduced to extinction by the phage, transferring the intracellular nitrogen held by Nodularia to Chlorella and rotifers, and allowing Chlorella to dominate the communities and rotifers to survive. This study shows that even though phages represent minuscule biomass, they can have key effects on community composition and eco-evolutionary feedbacks in plankton communities.

Nutrients from salmon parents alter selection pressures on their offspring.

Organisms can modify their surrounding environment, but whether these changes are large enough to feed back and alter their evolutionary trajectories is not well understood, particularly in wild populations. Here we show that nutrient pulses from decomposing Atlantic salmon (Salmo salar) parents alter selection pressures on their offspring with important consequences for their phenotypic and genetic diversity. We found a strong survival advantage to larger eggs and faster juvenile metabolic rates in streams lacking carcasses but not in streams containing this parental nutrient input. Differences in selection intensities led to significant phenotypic divergence in these two traits among stream types. Stronger selection in streams with low parental nutrient input also decreased the number of surviving families compared to streams with high parental nutrient levels. Observed effects of parent-derived nutrients on selection pressures provide experimental evidence for key components of eco-evolutionary feedbacks in wild populations.

CO2 studies remain key to understanding a future world.

Contents 34 I. 34 II. 36 III. 37 IV. 37 V. 38 38 References 38 SUMMARY: Characterizing plant responses to past, present and future changes in atmospheric carbon dioxide concentration ([CO2 ]) is critical for understanding and predicting the consequences of global change over evolutionary and ecological timescales. Previous CO2 studies have provided great insights into the effects of rising [CO2 ] on leaf-level gas exchange, carbohydrate dynamics and plant growth. However, scaling CO2 effects across biological levels, especially in field settings, has proved challenging. Moreover, many questions remain about the fundamental molecular mechanisms driving plant responses to [CO2 ] and other global change factors. Here we discuss three examples of topics in which significant questions in CO2 research remain unresolved: (1) mechanisms of CO2 effects on plant developmental transitions; (2) implications of rising [CO2 ] for integrated plant-water dynamics and drought tolerance; and (3) CO2 effects on symbiotic interactions and eco-evolutionary feedbacks. Addressing these and other key questions in CO2 research will require collaborations across scientific disciplines and new approaches that link molecular mechanisms to complex physiological and ecological interactions across spatiotemporal scales.

Antagonistic coevolution between quantitative and Mendelian traits.

Coevolution is relentlessly creating and maintaining biodiversity and therefore has been a central topic in evolutionary biology. Previous theoretical studies have mostly considered coevolution between genetically symmetric traits (i.e. coevolution between two continuous quantitative traits or two discrete Mendelian traits). However, recent empirical evidence indicates that coevolution can occur between genetically asymmetric traits (e.g. between quantitative and Mendelian traits). We examine consequences of antagonistic coevolution mediated by a quantitative predator trait and a Mendelian prey trait, such that predation is more intense with decreased phenotypic distance between their traits (phenotype matching). This antagonistic coevolution produces a complex pattern of bifurcations with bistability (initial state dependence) in a two-dimensional model for trait coevolution. Furthermore, with eco-evolutionary dynamics (so that the trait evolution affects predator-prey population dynamics), we find that coevolution can cause rich dynamics including anti-phase cycles, in-phase cycles, chaotic dynamics and deterministic predator extinction. Predator extinction is more likely to occur when the prey trait exhibits complete dominance rather than semidominance and when the predator trait evolves very rapidly. Our study illustrates how recognizing the genetic architectures of interacting ecological traits can be essential for understanding the population and evolutionary dynamics of coevolving species.

How Ecology and Landscape Dynamics Shape Phylogenetic Trees.

Whether biotic or abiotic factors are the dominant drivers of clade diversification is a long-standing question in evolutionary biology. The ubiquitous patterns of phylogenetic imbalance and branching slowdown have been taken as supporting the role of ecological niche filling and spatial heterogeneity in ecological features, and thus of biotic processes, in diversification. However, a proper theoretical assessment of the relative roles of biotic and abiotic factors in macroevolution requires models that integrate both types of factors, and such models have been lacking. In this study, we use an individual-based model to investigate the temporal patterns of diversification driven by ecological speciation in a stochastically fluctuating geographic landscape. The model generates phylogenies whose shape evolves as the clade ages. Stabilization of tree shape often occurs after ecological saturation, revealing species turnover caused by competition and demographic stochasticity. In the initial phase of diversification (allopatric radiation into an empty landscape), trees tend to be unbalanced and branching slows down. As diversification proceeds further due to landscape dynamics, balance and branching tempo may increase and become positive. Three main conclusions follow. First, the phylogenies of ecologically saturated clades do not always exhibit branching slowdown. Branching slowdown requires that competition be wide or heterogeneous across the landscape, or that the characteristics of landscape dynamics vary geographically. Conversely, branching acceleration is predicted under narrow competition or frequent local catastrophes. Second, ecological heterogeneity does not necessarily cause phylogenies to be unbalanced--short time in geographical isolation or frequent local catastrophes may lead to balanced trees despite spatial heterogeneity. Conversely, unbalanced trees can emerge without spatial heterogeneity, notably if competition is wide. Third, short isolation time causes a radically different and quite robust pattern of phylogenies that are balanced and yet exhibit branching slowdown. In conclusion, biotic factors have a strong and diverse influence on the shape of phylogenies of ecologically saturating clades and create the evolutionary template in which branching slowdown and tree imbalance may occur. However, the contingency of landscape dynamics and resource distribution can cause wide variation in branching tempo and tree balance. Finally, considerable variation in tree shape among simulation replicates calls for caution when interpreting variation in the shape of real phylogenies.

Population size-structure-dependent fitness and ecosystem consequences in Trinidadian guppies.

Decades of theory and recent empirical results have shown that evolutionary, population, community and ecosystem properties are the result of feedbacks between ecological and evolutionary processes. The vast majority of theory and empirical research on these eco-evolutionary feedbacks has focused on interactions among population size and mean traits of populations. However, numbers and mean traits represent only a fraction of the possible feedback dimensions. Populations of many organisms consist of different size classes that differ in their impact on the environment and each other. Moreover, rarely do we know the map of ecological pathways through which changes in numbers or size structure cause evolutionary change. The goal of this study was to test the role of size structure in eco-evolutionary feedbacks of Trinidadian guppies and to begin to build an eco-evolutionary map along this unexplored dimension. We used a factorial experiment in mesocosms wherein we crossed high- and low-predation guppy phenotypes with population size structure. We tested the ability of changes in size structure to generate selection on the demographic rates of guppies using an integral projection model (IPM). To understand how fitness differences among high- and low-predation phenotypes may be generated, we measured the response of the biomass of lower trophic levels and nutrient cycling to the different phenotype and size structure treatments. We found a significant interaction between guppy phenotype and the size structure treatments for absolute fitness. Size structure had a very large effect on invertebrate biomass in the mesocosms, but there was little or no effect of the phenotype. The effect of size structure on algal biomass depended on guppy phenotype, with no difference in algal biomass in populations with more, smaller guppies, but a large decrease in algal biomass in mesocosms with phenotypes adapted to low-predation risk. These results indicate an important role for size structure partially driving eco-evolutionary feedbacks in guppies. The changes in the ecosystem suggest that the absence of a steep decline in guppy fitness of the low-predation risk populations is likely due to higher consumption of algae when invertebrates are comparatively rare. Overall, these results demonstrate size structure as a possible dimension through which eco-evolutionary feedbacks may occur in natural populations.

Effects of local negative feedbacks on the evolution of species within metacommunities.

Local negative feedbacks occur when the occupation of a site by a species decreases the subsequent fitness of related individuals compared to potential competitors. Such negative feedbacks can enhance diversity by changing the spatial structure of the environment. The conditions, however, involve dispersive, environmental and evolutionary processes in complex interactive ways. We introduce a model that accounts for four mechanisms: colonisation-competition-extinction ecological dynamics, evolutionary dynamics, local negative feedbacks and environmental averaging. Three qualitatively distinct dynamics are possible, one dominated by specialists, another dominated by generalists and an intermediate situation exhibiting taxon cycles. We discuss how metacommunity diversity, macro-ecological patterns and environmental patterning are linked to the three qualitative dynamics. The model provides classical shapes for morph-abundance distributions, or diversity-area relationships. Diversity can be high when specialists dominate or when taxon cycles happen. Finally, local negative feedbacks often yield fine-grain environments for taxon cycle dynamics and coarse-grain environments when generalists dominate.

The eco-evolutionary origins of life.

The origin of life remains one of the greatest enigmas in science. The immense leap in complexity between prebiotic soup and cellular life challenges historically "chemistry-forward" and "biology-backwards" approaches. Evolution must have bridged this gap in complexity, so understanding factors that influence evolutionary outcomes is critical for exploring life's emergence. Here, we review insights from ecology and evolution and their application throughout abiogenesis. In particular, we discuss how ecological and evolutionary constraints shape the evolution of biological innovation. We propose an "eco-evolutionary" approach, which is agnostic towards particular chemistries or environments and instead explores the several ways that an evolvable system may emerge and gain complexity.