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.

Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics.

The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions-one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems.

The role of fish predators and their foraging traits in shaping zooplankton community structure.

Differentiation of foraging traits among predator populations may help explain observed variation in the structure of prey communities. However, few studies have investigated the phenotypic effects of predators on their prey in natural communities. Here, we use a comparative analysis of 78 Greenlandic lakes to examine how foraging trait variation among threespine stickleback populations can help explain variation in zooplankton community composition among lakes. We find that landscape-scale variation in zooplankton composition was jointly explained by lake properties, such as size and water chemistry, and the presence and absence of both stickleback and arctic char. Additional variation in zooplankton community structure can be explained by stickleback jaw protrusion, a trait with known utility for foraging on zooplankton, but only in lakes where stickleback co-occur with arctic char. Overall, our results illustrate how trait variation of predators, alongside other ecosystem properties, can influence the composition of prey communities in nature.

Evolution of realized niche breadth diversity driven by community dynamics.

Why many herbivorous insects are host plant specialists, with non-negligible exceptions, is a conundrum of evolutionary biology, especially because the host plants are not necessarily optimal larval diets. Here, I present a novel model of host plant preference evolution of two insect species. Because habitat preference evolution is contingent upon demographic dynamics, I integrate the evolutionary framework with the modern coexistence theory. The results show that the two insect species can evolve into a habitat specialist and generalist, when they experience both negative and positive frequency-dependent community dynamics. This happens because the joint action of positive and negative frequency dependence creates multiple (up to nine) eco-evolutionary equilibria. Furthermore, initial condition dependence due to positive frequency dependence allows specialization to poor habitats. Thus, evolved habitat preferences do not necessarily correlate with the performances. The model provides explanations for counterintuitive empirical patterns and mechanistic interpretations for phenomenological models of niche breadth evolution.

Range expansion is both slower and more variable with rapid evolution across a spatial gradient in temperature.

Rapid evolution in colonising populations can alter our ability to predict future range expansions. Recent theory suggests that the dynamics of replicate range expansions are less variable, and hence more predictable, with increased selection at the expanding range front. Here, we test whether selection from environmental gradients across space produces more consistent range expansion speeds, using the experimental evolution of replicate duckweed populations colonising landscapes with and without a temperature gradient. We found that the range expansion across a temperature gradient was slower on average, with range-front populations displaying higher population densities, and genetic signatures and trait changes consistent with directional selection. Despite this, we found that with a spatial gradient range expansion speed became more variable and less consistent among replicates over time. Our results therefore challenge current theory, highlighting that chance can still shape the genetic response to selection to influence our ability to predict range expansion speeds.

Evolutionary rescue in resistance to pesticides.

Evolutionary rescue occurs when the genetic evolution of adaptation saves a population from decline or extinction after environmental change. The evolution of resistance to pesticides is a special scenario of abrupt environmental change, where rescue occurs under (very) strong selection for one or a few de novo resistance mutations of large effect. Here, a population genetic model of evolutionary rescue with density-dependent population change is developed, with a focus on deriving results that are important to resistance management. Massive stochastic simulations are used to generate observations, which are accurately predicted using analytical approximations. Key results include the probability density function for the time to resistance and the probability of population extinction. The distribution of resistance times shows a lag period, a narrow peak and a long tail. Surprisingly, the mean time to resistance can increase with the strength of selection because, if a mutation does not occur early on, then its emergence is delayed by the pesticide reducing the population size. The probability of population extinction shows a sharp transition, in that when extinction is possible, it is also highly likely. Consequently, population suppression and (local) eradication can be theoretically achievable goals, as novel strategies to delay resistance evolution.

Modelling optimal ligninolytic activity during plant litter decomposition.

A large fraction of plant litter comprises recalcitrant aromatic compounds (lignin and other phenolics). Quantifying the fate of aromatic compounds is difficult, because oxidative degradation of aromatic carbon (C) is a costly but necessary endeavor for microorganisms, and we do not know when gains from the decomposition of aromatic C outweigh energetic costs. To evaluate these tradeoffs, we developed a litter decomposition model in which the aromatic C decomposition rate is optimized dynamically to maximize microbial growth for the given costs of maintaining ligninolytic activity. We tested model performance against > 200 litter decomposition datasets collected from published literature and assessed the effects of climate and litter chemistry on litter decomposition. The model predicted a time-varying ligninolytic oxidation rate, which was used to calculate the lag time before the decomposition of aromatic C is initiated. Warmer conditions increased decomposition rates, shortened the lag time of aromatic C oxidation, and improved microbial C-use efficiency by decreasing the costs of oxidation. Moreover, a higher initial content of aromatic C promoted an earlier start of aromatic C decomposition under any climate. With this contribution, we highlight the application of eco-evolutionary approaches based on optimized microbial life strategies as an alternative parametrization scheme for litter decomposition models.

'Drifting' Buchnera genomes track the microevolutionary trajectories of their aphid hosts.

Evolution of Buchnera-aphid host symbioses is often studied among species at macroevolutionary scales. Investigations within species offer a different perspective about how eco-evolutionary processes shape patterns of genetic variation at microevolutionary scales. Our study leverages new and publicly available whole-genome sequencing data to study Buchnera-aphid host evolution in Myzus persicae, the peach potato aphid, a globally invasive and polyphagous pest. Across 43 different asexual, clonally reproducing isofemale strains, we examined patterns of genomic covariation between Buchnera and their aphid host and considered the distribution of mutations in protein-coding regions of the Buchnera genome. We found Buchnera polymorphisms within aphid strains, suggesting the presence of genetically different Buchnera strains within the same clonal lineage. Genetic distance between pairs of Buchnera samples was positively correlated to genetic distance between their aphid hosts, indicating shared evolutionary histories. However, there was no segregation of genetic variation for both M. persicae and Buchnera with plant host (Brassicaceae and non-tobacco Solanaceae) and no associations between genetic and geographic distance at global or regional spatial scales. Abundance patterns of non-synonymous mutations were similar to synonymous mutations in the Buchnera genome, and both mutation classes had similar site frequency spectra. We hypothesize that a predominance of neutral processes results in the Buchnera of M. persicae to simply 'drift' with the evolutionary trajectory of their aphid hosts. Our study presents a unique microevolutionary characterization of Buchnera-aphid host genomic covariation across multiple aphid clones. This provides a new perspective on the eco-evolutionary processes generating and maintaining polymorphisms in a major pest aphid species and its obligate primary endosymbiont.

Stability, resilience and eco-evolutionary feedbacks of mutualistic networks to rising temperature.

Ecological networks comprising of mutualistic interactions can suddenly transition to undesirable states, such as collapse, due to small changes in environmental conditions such as a rise in local environmental temperature. However, little is known about the capacity of such interaction networks to adapt to a rise in temperature and the occurrence of critical transitions. Here, combining quantitative genetics and mutualistic dynamics in an eco-evolutionary framework, we evaluated the stability and resilience of mutualistic networks to critical transitions as environmental temperature increases. Specifically, we modelled the dynamics of an optimum trait that determined the tolerance of species to local environmental temperature as well as to species interaction. We then evaluated the impact of individual trait variation and evolutionary dynamics on the stability of feasible equilibria, the occurrence of threshold temperatures at which community collapses, and the abruptness of such community collapses. We found that mutualistic network architecture, that is the size of the community and the arrangement of species interactions, interacted with evolutionary dynamics to impact the onset of network collapses. Some networks had more capacity to track the rise in temperatures than others and thereby increased the threshold temperature at which the networks collapsed. However, such a result was modulated by the amount of heritable trait variation species exhibited, with high trait variation in the mean optimum phenotypic trait increasing the environmental temperature at which networks collapsed. Furthermore, trait variation not only increased the onset of temperatures at which networks collapsed but also increased the local stability of feasible equilibria. Our study argued that mutualistic network architecture interacts with species evolutionary dynamics and increases the capacity of networks to adapt to changes in temperature and thereby delayed the occurrence of community collapses.

Mutualism at the leading edge: insights into the eco-evolutionary dynamics of host-symbiont communities during range expansion.

The evolution of mutualism between host and symbiont communities plays an essential role in maintaining ecosystem function and should therefore have a profound effect on their range expansion dynamics. In particular, the presence of mutualistic symbionts at the leading edge of a host-symbiont community should enhance its propagation in space. We develop a theoretical framework that captures the eco-evolutionary dynamics of host-symbiont communities, to investigate how the evolution of resource exchange may shape community structure during range expansion. We consider a community with symbionts that are mutualistic or parasitic to various degrees, where parasitic symbionts receive the same amount of resource from the host as mutualistic symbionts, but at a lower cost. The selective advantage of parasitic symbionts over mutualistic ones is increased with resource availability (i.e. with host density), promoting mutualism at the range edges, where host density is low, and parasitism at the population core, where host density is higher. This spatial selection also influences the speed of spread. We find that the host growth rate (which depends on the average benefit provided by the symbionts) is maximal at the range edges, where symbionts are more mutualistic, and that host-symbiont communities with high symbiont density at their core (e.g. resulting from more mutualistic hosts) spread faster into new territories. These results indicate that the expansion of host-symbiont communities is pulled by the hosts but pushed by the symbionts, in a unique push-pull dynamic where both the host and symbionts are active and tightly-linked players.

Growth-defense trade-offs shape population genetic composition in an iconic forest tree species.

All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal, Annu. Rev. Plant Biol., 68, 513-534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth-defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipollini et al., Annual Plant Reviews (Wiley, 2014), pp. 263-307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth-defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fast-growing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunner et al., Funct. Ecol. 33, 7-12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.

Coevolution of species colonisation rates controls food-chain length in spatially structured food webs.

How the complexity of food webs depends on environmental variables is a long-standing ecological question. It is unclear though how food-chain length should vary with adaptive evolution of the constitutive species. Here we model the evolution of species colonisation rates and its consequences on occupancies and food-chain length in metacommunities. When colonisation rates can evolve, longer food-chains can persist. Extinction, perturbation and habitat loss all affect evolutionarily stable colonisation rates, but the strength of the competition-colonisation trade-off has a major role: weaker trade-offs yield longer chains. Although such eco-evo dynamics partly alleviates the spatial constraint on food-chain length, it is no magic bullet: the highest, most vulnerable, trophic levels are also those that least benefit from evolution. We provide qualitative predictions regarding how trait evolution affects the response of communities to disturbance and habitat loss. This highlights the importance of eco-evolutionary dynamics at metacommunity level in determining food-chain length.

Incorporating ecology into gene drive modelling.

Gene drive technology, in which fast-spreading engineered drive alleles are introduced into wild populations, represents a promising new tool in the fight against vector-borne diseases, agricultural pests and invasive species. Due to the risks involved, gene drives have so far only been tested in laboratory settings while their population-level behaviour is mainly studied using mathematical and computational models. The spread of a gene drive is a rapid evolutionary process that occurs over timescales similar to many ecological processes. This can potentially generate strong eco-evolutionary feedback that could profoundly affect the dynamics and outcome of a gene drive release. We, therefore, argue for the importance of incorporating ecological features into gene drive models. We describe the key ecological features that could affect gene drive behaviour, such as population structure, life-history, environmental variation and mode of selection. We review previous gene drive modelling efforts and identify areas where further research is needed. As gene drive technology approaches the level of field experimentation, it is crucial to evaluate gene drive dynamics, potential outcomes, and risks realistically by including ecological processes.

Contemporary changes in phenotypic variation, and the potential consequences for eco-evolutionary dynamics.

Most studies assessing rates of phenotypic change focus on population mean trait values, whereas a largely overlooked additional component is changes in population trait variation. Theoretically, eco-evolutionary dynamics mediated by such changes in trait variation could be as important as those mediated by changes in trait means. To date, however, no study has comprehensively summarised how phenotypic variation is changing in contemporary populations. Here, we explore four questions using a large database: How do changes in trait variances compare to changes in trait means? Do different human disturbances have different effects on trait variance? Do different trait types have different effects on changes in trait variance? Do studies that established a genetic basis for trait change show different patterns from those that did not? We find that changes in variation are typically small; yet we also see some very large changes associated with particular disturbances or trait types. We close by interpreting and discussing the implications of our findings in the context of eco-evolutionary studies.

The significance of partial migration for food web and ecosystem dynamics.

Migration is ubiquitous and can strongly shape food webs and ecosystems. Less familiar, however, is that the majority of life cycle, seasonal and diel migrations in nature are partial migrations: only a fraction of the population migrates while the other individuals remain in their resident ecosystem. Here, we demonstrate different impacts of partial migration rendering it fundamental to our understanding of the significance of migration for food web and ecosystem dynamics. First, partial migration affects the spatiotemporal distribution of individuals and the food web and ecosystem-level processes they drive differently than expected under full migration. Second, whether an individual migrates or not is regularly correlated with morphological, physiological, and/or behavioural traits that shape its food-web and ecosystem-level impacts. Third, food web and ecosystem dynamics can drive the fraction of the population migrating, enabling the potential for feedbacks between the causes and consequences of migration within and across ecosystems. These impacts, individually and in combination, can yield unintuitive effects of migration and drive the dynamics, diversity and functions of ecosystems. By presenting the first full integration of partial migration and trophic (meta-)community and (meta-)ecosystem ecology, we provide a roadmap for studying how migration affects and is affected by ecosystem dynamics in a changing world.

Extending eco-evolutionary theory with oligomorphic dynamics.

Understanding the interplay between ecological processes and the evolutionary dynamics of quantitative traits in natural systems remains a major challenge. Two main theoretical frameworks are used to address this question, adaptive dynamics and quantitative genetics, both of which have strengths and limitations and are often used by distinct research communities to address different questions. In order to make progress, new theoretical developments are needed that integrate these approaches and strengthen the link to empirical data. Here, we discuss a novel theoretical framework that bridges the gap between quantitative genetics and adaptive dynamics approaches. 'Oligomorphic dynamics' can be used to analyse eco-evolutionary dynamics across different time scales and extends quantitative genetics theory to account for multimodal trait distributions, the dynamical nature of genetic variance, the potential for disruptive selection due to ecological feedbacks, and the non-normal or skewed trait distributions encountered in nature. Oligomorphic dynamics explicitly takes into account the effect of environmental feedback, such as frequency- and density-dependent selection, on the dynamics of multi-modal trait distributions and we argue it has the potential to facilitate a much tighter integration between eco-evolutionary theory and empirical data.

Pushed to the edge: Spatial sorting can slow down invasions.

Our ability to understand population spread dynamics is complicated by rapid evolution, which renders simple ecological models insufficient. If dispersal ability evolves, more highly dispersive individuals may arrive at the population edge than less dispersive individuals (spatial sorting), accelerating spread. If individuals at the low-density population edge benefit (escape competition), high dispersers have a selective advantage (spatial selection). These two processes are often described as forming a positive feedback loop; they reinforce each other, leading to faster spread. Although spatial sorting is close to universal, this form of spatial selection is not: low densities can be detrimental for organisms with Allee effects. Here, we present two conceptual models to explore the feedback loops that form between spatial sorting and spatial selection. We show that the presence of an Allee effect can reverse the positive feedback loop between spatial sorting and spatial selection, creating a negative feedback loop that slows population spread.

Opportunities to advance the synthesis of ecology and evolution.

Despite decades of research on the interactions between ecology and evolution, opportunities still remain to further integrate the two disciplines, especially when considering multispecies systems. Here, we discuss two such opportunities. First, the traditional emphasis on the distinction between evolutionary and ecological processes should be further relaxed as it is particularly unhelpful in the study of microbial communities, where the very notion of species is hard to define. Second, key processes of evolutionary theory such as adaptation should be exported to hierarchical levels higher than populations to make sense of biodiversity dynamics. Together, we argue that broadening our perspective of eco-evolutionary dynamics to be more inclusive of all biodiversity, both phylogenetically and hierarchically, will open up fertile new research directions and help us to address one of the major scientific challenges of our time, that is, to understand and predict changes in biodiversity in the face of rapid environmental change.

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.

What Can Evolutionary History Tell Us about the Functioning of Ecological Communities? The ASN Presidential Debate.

AbstractIn January 2018, Sharon Strauss, then president of the American Society of Naturalists, organized a debate on the following topic: does evolutionary history inform the current functioning of ecological communities? The debaters-Ives, Lau, Mayfield, and Tobias-presented pro and con arguments, caricatured in standard debating format. Numerous examples show that both recent microevolutionary and longer-term macroevolutionary history are important to the ecological functioning of communities. On the other hand, many other examples illustrate that the evolutionary history of communities or community members does not influence ecological function, or at least not very much. This article aims to provide a provocative discussion of the consistent and conflicting patterns that emerge in the study of contemporary and historical evolutionary influences on community function, as well as to identify questions for further study. It is intended as a thought-provoking exercise to explore this complex field, specifically addressing (1) key assumptions and how they can lead us astray and (2) issues that need additional study. The debaters all agree that evolutionary history can inform us about at least some aspects of community function. The underlying question at the root of the debate, however, is how the fields of ecology and evolution can most profitably collaborate to provide a deeper and broader understanding of ecological communities.