Evolution of ontogenetic niches promotes species coexistence in a surprising way.

Animals usually change their trophic niche during their ontogeny, which has fundamental consequences for their population dynamics and interactions with other species. Theory predicts that ontogenetic niche differences between species can influence their ability to coexist. However, we lack empirical evidence for this coexistence mechanism and the role of evolution in shaping species' ontogenetic niches. Here, Anaya-Rojas et al. (2023) show that contemporary evolution of ontogenetic niches likely contributes to the coexistence of two competing fish species (killifish and guppies) in streams on the Caribbean Island of Trinidad. As predicted by coexistence theory, they found that the weaker competitor (killifish) exhibited a relatively large ontogenetic niche shift, feeding at higher trophic levels as it grew, in streams where competition with the stronger competitor (guppies) was intense. Intuition suggests that the weaker competitor should experience strong selection on its ontogenetic niche in a different competitive environment, but this was not the case. Instead, they found that the stronger competitor evolved a more compressed ontogenetic niche, where guppies fed at a low trophic level regardless of their body size, when competition was intense. Although the mechanism underlying this surprising result remains to be determined, this work points to the importance of taking a food web perspective-explicitly accounting for consumer-resource interactions-to understand the outcome of eco-evolutionary dynamics. Given that ontogenetic niche shifts are extremely common in animals, understanding the evolutionary ecology of these niche shifts should be a priority for future research on species coexistence.

Genome-wide association study of aphid abundance highlights a locus affecting plant growth and flowering in Arabidopsis thaliana.

Plant life-history traits, such as size and flowering, contribute to shaping variation in herbivore abundance. Although plant genes involved in physical and chemical traits have been well studied, less is known about the loci linking plant life-history traits and herbivore abundance. Here, we conducted a genome-wide association study (GWAS) of aphid abundance in a field population of Arabidopsis thaliana. This GWAS of aphid abundance detected a relatively rare but significant variant on the third chromosome of A. thaliana, which was also suggestively but non-significantly associated with the presence or absence of inflorescence. Out of candidate genes near this significant variant, a mutant of a ribosomal gene (AT3G13882) exhibited slower growth and later flowering than a wild type under laboratory conditions. A no-choice assay with the turnip aphid, Lipaphis erysimi, found that aphids were unable to successfully establish on the mutant. Our GWAS of aphid abundance unexpectedly found a locus affecting plant growth and flowering.

Individual Dietary Specialization in a Generalist Bee Varies across Populations but Has No Effect on the Richness of Associated Microbial Communities.

AbstractDespite the increasingly documented occurrence of individual specialization, the relationship between individual consumer interactions and diet-related microbial communities in wild populations is still unclear. Using data from nests of Ceratina australensis from three different wild bee populations, we combine metabarcoding and network approaches to explore the existence of individual variation in resource use within and across populations and whether dietary specialization affects the richness of pollen-associated microbes. We reveal the existence of marked dietary specialization. In the most specialized population, we also show that individuals' diet breadth was positively related to the richness of fungi but not bacteria. Overall, individual specialization appeared to have a weak or negligible effect on the microbial richness of nests, suggesting that different mechanisms beyond environmental transmission may be at play regarding microbial acquisition in wild bees.

A keystone gene underlies the persistence of an experimental food web.

Genes encode information that determines an organism's fitness. Yet we know little about whether genes of one species influence the persistence of interacting species in an ecological community. Here, we experimentally tested the effect of three plant defense genes on the persistence of an insect food web and found that a single allele at a single gene promoted coexistence by increasing plant growth rate, which in turn increased the intrinsic growth rates of species across multiple trophic levels. Our discovery of a "keystone gene" illustrates the need to bridge between biological scales, from genes to ecosystems, to understand community persistence.

An Empiricist's Guide to Using Ecological Theory.

AbstractA scientific understanding of the biological world arises when ideas about how nature works are formalized, tested, refined, and then tested again. Although the benefits of feedback between theoretical and empirical research are widely acknowledged by ecologists, this link is still not as strong as it could be in ecological research. This is in part because theory, particularly when expressed mathematically, can feel inaccessible to empiricists who may have little formal training in advanced math. To address this persistent barrier, we provide a general and accessible guide that covers the basic, step-by-step process of how to approach, understand, and use ecological theory in empirical work. We first give an overview of how and why mathematical theory is created, then outline four specific ways to use both mathematical and verbal theory to motivate empirical work, and finally present a practical tool kit for reading and understanding the mathematical aspects of ecological theory. We hope that empowering empiricists to embrace theory in their work will help move the field closer to a full integration of theoretical and empirical research.

Genetic and plastic rewiring of food webs under climate change.

Climate change is altering ecological and evolutionary processes across biological scales. These simultaneous effects of climate change pose a major challenge for predicting the future state of populations, communities and ecosystems. This challenge is further exacerbated by the current lack of integration of research focused on these different scales. We propose that integrating the fields of quantitative genetics and food web ecology will reveal new insights on how climate change may reorganize biodiversity across levels of organization. This is because quantitative genetics links the genotypes of individuals to population-level phenotypic variation due to genetic (G), environmental (E) and gene-by-environment (G × E) factors. Food web ecology, on the other hand, links population-level phenotypes to the structure and dynamics of communities and ecosystems. We synthesize data and theory across these fields and find evidence that genetic (G) and plastic (E and G × E) phenotypic variation within populations will change in magnitude under new climates in predictable ways. We then show how changes in these sources of phenotypic variation can rewire food webs by altering the number and strength of species interactions, with consequences for ecosystem resilience. We also find evidence suggesting there are predictable asymmetries in genetic and plastic trait variation across trophic levels, which set the pace for phenotypic change and food web responses to climate change. Advances in genomics now make it possible to partition G, E and G × E phenotypic variation in natural populations, allowing tests of the hypotheses we propose. By synthesizing advances in quantitative genetics and food web ecology, we provide testable predictions for how the structure and dynamics of biodiversity will respond to climate change.

Ecological Character Displacement Destabilizes Food Webs.

AbstractEcological character displacement is an adaptive process that generally increases phenotypic diversity. Despite the fact that this diversification is due to an eco-evolutionary feedback between consumers competing for shared resources, its consequences for food-web dynamics have received little attention. Here, I study a model of two consumers competing for two shared resources to examine how character displacement in consumer attack rates affects resource abundances and the resilience of food webs to perturbations. I found that character displacement always strengthened consumer-resource interactions whenever consumers competed for resources that occurred in different habitats. This increase in interaction strength resulted in lower resource abundances and less resilient food webs. This occurred under different evolutionary trade-offs and in both simple and more realistic foraging scenarios. Taken together, my results show that the adaptive process of character displacement may come with the ecological cost of decreasing food-web resilience.

Partner Fidelity and Asymmetric Specialization in Ecological Networks.

AbstractSpecies are embedded in complex networks of interdependencies that may change across geographic locations. Yet most approaches to investigate the architecture of this entangled web of life have considered exclusively local communities. To quantify to what extent species interactions change at a biogeographic scale, we need to shed light on how among-community variation affects the occurrence of species interactions. Here we quantify the probability for two partners to interact wherever they co-occur (i.e., partner fidelity) by analyzing the most extensive database on species interaction networks worldwide. We found that mutualistic species show more fidelity in their interactions than antagonistic ones when there is asymmetric specialization (i.e., when specialist species interact with generalist partners). Moreover, resources (e.g., plants in plant-pollinator mutualisms or hosts in host-parasite interactions) show a higher partner fidelity in mutualistic interactions than in antagonistic interactions, which can be explained neither by sampling effort nor by phylogenetic constraints developed during their evolutionary histories. In spite of the general belief that mutualistic interactions among free-living species are labile, asymmetric specialization is very much conserved across large geographic areas.

Loss of consumers constrains phenotypic evolution in the resulting food web.

The loss of biodiversity is altering the structure of ecological networks; however, we are currently in a poor position to predict how these altered communities will affect the evolution of remaining populations. Theory on fitness landscapes provides a framework for predicting how selection alters the evolutionary trajectory and adaptive potential of populations, but often treats the network of interacting populations as a "black box." Here, we integrate ecological networks and fitness landscapes to examine how changes in food-web structure shape phenotypic evolution. We conducted a field experiment that removed a guild of larval parasitoids that imposed direct and indirect selection pressures on an insect herbivore. We then measured herbivore survival as a function of three key phenotypic traits to estimate directional, quadratic, and correlational selection gradients in each treatment. We used these selection gradients to characterize the slope and curvature of the fitness landscape to understand the direct and indirect effects of consumer loss on phenotypic evolution. We found that the number of traits under directional selection increased with the removal of larval parasitoids, indicating evolution was more constrained toward a specific combination of traits. Similarly, we found that the removal of larval parasitoids altered the curvature of the fitness landscape in such a way that tended to decrease the evolvability of the traits we measured in the next generation. Our results suggest that the loss of trophic interactions can impose greater constraints on phenotypic evolution. This indicates that the simplification of ecological communities may constrain the adaptive potential of remaining populations to future environmental change.

Urbanization reshapes a food web.

Cities represent humanity's most intense impact on our planet, with more than half of all humans now residing in urban areas. Indeed, urbanization has well-understood impacts on both individual species and general patterns of biodiversity. However, species do not exist in isolation, but are instead members of complex interaction networks that shape patterns of diversity and influence ecosystem services. Despite the importance of species interaction for creating patterns of diversity, we do not understand how urbanization alters these interactions. Here, we investigate how an interaction network (food web) is reshaped by urbanization. We show that, consistent with theory, cities tend to support less diverse ecological communities, and rare species that interact with few species are particularly sensitive to urbanization. As a result, remnant urban food webs tend to have more interactions per species and greater connectance, creating more integrated interaction networks. We discuss the implications of this food web reshaping for ecological stability, eco-evolutionary dynamics, and the joining of interaction networks and conservation planning. The role of cities in reshaping interaction networks provides an interesting study of food web (dis)assembly, while also shedding light on new approaches to applied conservation issues.

Coevolutionary dynamics shape the structure of bacteria-phage infection networks.

Coevolution-reciprocal evolutionary change among interacting species driven by natural selection-is thought to be an important force in shaping biodiversity. This ongoing process takes place within tangled networks of species interactions. In microbial communities, evolutionary change between hosts and parasites occurs at the same time scale as ecological change. Yet, we still lack experimental evidence of the role of coevolution in driving changes in the structure of such species interaction networks. Filling this gap is important because network structure influences community persistence through indirect effects. Here, we quantified experimentally to what extent coevolutionary dynamics lead to contrasting patterns in the architecture of bacteria-phage infection networks. Specifically, we look at the tendency of these networks to be organized in a nested pattern by which the more specialist phages tend to infect only a proper subset of those bacteria infected by the most generalist phages. We found that interactions between coevolving bacteria and phages become less nested over time under fluctuating dynamics, and more nested under arms race dynamics. Moreover, when coevolution results in high average infectivity, phages and bacteria differ more from each other over time under arms race dynamics than under fluctuating dynamics. The tradeoff between the fitness benefits of evolving resistance/infectivity traits and the costs of maintaining them might explain these differences in network structure. Our study shows that the interaction pattern between bacteria and phages at the community level depends on the way coevolution unfolds.

Caught in the web: Spider web architecture affects prey specialization and spider-prey stoichiometric relationships.

Quantitative approaches to predator-prey interactions are central to understanding the structure of food webs and their dynamics. Different predatory strategies may influence the occurrence and strength of trophic interactions likely affecting the rates and magnitudes of energy and nutrient transfer between trophic levels and stoichiometry of predator-prey interactions. Here, we used spider-prey interactions as a model system to investigate whether different spider web architectures-orb, tangle, and sheet-tangle-affect the composition and diet breadth of spiders and whether these, in turn, influence stoichiometric relationships between spiders and their prey. Our results showed that web architecture partially affects the richness and composition of the prey captured by spiders. Tangle-web spiders were specialists, capturing a restricted subset of the prey community (primarily Diptera), whereas orb and sheet-tangle web spiders were generalists, capturing a broader range of prey types. We also observed elemental imbalances between spiders and their prey. In general, spiders had higher requirements for both nitrogen (N) and phosphorus (P) than those provided by their prey even after accounting for prey biomass. Larger P imbalances for tangle-web spiders than for orb and sheet-tangle web spiders suggest that trophic specialization may impose strong elemental constraints for these predators unless they display behavioral or physiological mechanisms to cope with nutrient limitation. Our findings suggest that integrating quantitative analysis of species interactions with elemental stoichiometry can help to better understand the occurrence of stoichiometric imbalances in predator-prey interactions.

What genomic data can reveal about eco-evolutionary dynamics.

Recognition that evolution operates on the same timescale as ecological processes has motivated growing interest in eco-evolutionary dynamics. Nonetheless, generating sufficient data to test predictions about eco-evolutionary dynamics has proved challenging, particularly in natural contexts. Here we argue that genomic data can be integrated into the study of eco-evolutionary dynamics in ways that deepen our understanding of the interplay between ecology and evolution. Specifically, we outline five major questions in the study of eco-evolutionary dynamics for which genomic data may provide answers. Although genomic data alone will not be sufficient to resolve these challenges, integrating genomic data can provide a more mechanistic understanding of the causes of phenotypic change, help elucidate the mechanisms driving eco-evolutionary dynamics, and lead to more accurate evolutionary predictions of eco-evolutionary dynamics in nature.

Warming-Induced Changes to Body Size Stabilize Consumer-Resource Dynamics.

Both body size and temperature directly influence consumer-resource dynamics. There is also widespread empirical evidence for the temperature-size rule (TSR), which creates a negative relationship between temperature and body size. However, it is not known how the TSR affects community dynamics. Here we integrate temperature- and size-dependent models to include indirect effects of warming, through changes in body size, to answer the question, How does the TSR affect the predicted response of consumer-resource systems to warming? We find that the TSR is expected to maintain consumer-resource biomass ratios and buffer the community from extinctions under warming. While our results are limited to conditions where organisms are below their thermal optimum, they hold under a range of realistic temperature-size responses and are robust to the type of functional response. Our analyses suggest that the widely observed TSR may reduce the impacts of warming on consumer-resource systems.

Genetic variation in resistance to leaf fungus indirectly affects spider density.

Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities.

Genetic specificity of a plant-insect food web: Implications for linking genetic variation to network complexity.

Theory predicts that intraspecific genetic variation can increase the complexity of an ecological network. To date, however, we are lacking empirical knowledge of the extent to which genetic variation determines the assembly of ecological networks, as well as how the gain or loss of genetic variation will affect network structure. To address this knowledge gap, we used a common garden experiment to quantify the extent to which heritable trait variation in a host plant determines the assembly of its associated insect food web (network of trophic interactions). We then used a resampling procedure to simulate the additive effects of genetic variation on overall food-web complexity. We found that trait variation among host-plant genotypes was associated with resistance to insect herbivores, which indirectly affected interactions between herbivores and their insect parasitoids. Direct and indirect genetic effects resulted in distinct compositions of trophic interactions associated with each host-plant genotype. Moreover, our simulations suggest that food-web complexity would increase by 20% over the range of genetic variation in the experimental population of host plants. Taken together, our results indicate that intraspecific genetic variation can play a key role in structuring ecological networks, which may in turn affect network persistence.

Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes.

Many species approach, inspect and signal towards their predators. These behaviours are often interpreted as predator-deterrent signals--honest signals that indicate to a predator that continued hunting is likely to be futile. However, many of these putative predator-deterrent signals are given when no predator is present, and it remains unclear if and why such signals deter predators. We examined the effects of one such signal, the tail-flag display of California ground squirrels, which is frequently given both during and outside direct encounters with northern Pacific rattlesnakes. We video-recorded and quantified the ambush foraging responses of rattlesnakes to tail-flagging displays from ground squirrels. We found that tail-flagging deterred snakes from striking squirrels, most likely by advertising squirrel vigilance (i.e. readiness to dodge a snake strike). We also found that tail-flagging by adult squirrels increased the likelihood that snakes would leave their ambush site, apparently by elevating the vigilance of nearby squirrels which reduces the profitability of the ambush site. Our results provide some of the first empirical evidence of the mechanisms by which a prey display, although frequently given in the absence of a predator, may still deter predators during encounters.