Predator mass mortality events restructure food webs through trophic decoupling.

Predators have a key role in structuring ecosystems1-4. However, predator loss is accelerating globally4-6, and predator mass-mortality events7 (MMEs)-rapid large-scale die-offs-are now emblematic of the Anthropocene epoch6. Owing to their rare and unpredictable nature7, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies2,3 may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse8, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses2,3 or resource pulses9 alone, but that can be predicted from theory8. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control1-3 and stronger bottom-up effects through predator decomposition8. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. These results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.

Diatom abundance in the polar oceans is predicted by genome size.

A principal goal in ecology is to identify the determinants of species abundances in nature. Body size has emerged as a fundamental and repeatable predictor of abundance, with smaller organisms occurring in greater numbers than larger ones. A biogeographic component, known as Bergmann's rule, describes the preponderance, across taxonomic groups, of larger-bodied organisms in colder areas. Although undeniably important, the extent to which body size is the key trait underlying these patterns is unclear. We explored these questions in diatoms, unicellular algae of global importance for their roles in carbon fixation and energy flow through marine food webs. Using a phylogenomic dataset from a single lineage with worldwide distribution, we found that body size (cell volume) was strongly correlated with genome size, which varied by 50-fold across species and was driven by differences in the amount of repetitive DNA. However, directional models identified temperature and genome size, not cell size, as having the greatest influence on maximum population growth rate. A global metabarcoding dataset further identified genome size as a strong predictor of species abundance in the ocean, but only in colder regions at high and low latitudes where diatoms with large genomes dominated, a pattern consistent with Bergmann's rule. Although species abundances are shaped by myriad interacting abiotic and biotic factors, genome size alone was a remarkably strong predictor of abundance. Taken together, these results highlight the cascading cellular and ecological consequences of macroevolutionary changes in an emergent trait, genome size, one of the most fundamental and irreducible properties of an organism.

Meta-analytical evidence for frequency-dependent selection across the tree of life.

Explaining the maintenance of genetic variation in fitness-related traits within populations is a fundamental challenge in ecology and evolutionary biology. Frequency-dependent selection (FDS) is one mechanism that can maintain such variation, especially when selection favours rare variants (negative FDS). However, our general knowledge about the occurrence of FDS, its strength and direction remain fragmented, limiting general inferences about this important evolutionary process. We systematically reviewed the published literature on FDS and assembled a database of 747 effect sizes from 101 studies to analyse the occurrence, strength, and direction of FDS, and the factors that could explain heterogeneity in FDS. Using a meta-analysis, we found that overall, FDS is more commonly negative, although not significantly when accounting for phylogeny. An analysis of absolute values of effect sizes, however, revealed the widespread occurrence of modest FDS. However, negative FDS was only significant in laboratory experiments and non-significant in mesocosms and field-based studies. Moreover, negative FDS was stronger in studies measuring fecundity and involving resource competition over studies using other fitness components or focused on other ecological interactions. Our study unveils key general patterns of FDS and points in future promising research directions that can help us understand a long-standing fundamental problem in evolutionary biology and its consequences for demography and ecological dynamics.

Resetting our expectations for parasites and their effects on species interactions: a meta-analysis.

Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host-species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta-analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non-parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host-species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically-transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non-parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.

Interactions between fitness components across the life cycle constrain competitor coexistence.

Numerous mechanisms can promote competitor coexistence. Yet, these mechanisms are often considered in isolation from one another. Consequently, whether multiple mechanisms shaping coexistence combine to promote or constrain species coexistence remains an open question. Here, we aim to understand how multiple mechanisms interact within and between life stages to determine frequency-dependent population growth, which has a key role stabilizing local competitor coexistence. We conducted field experiments in three lakes manipulating relative frequencies of two Enallagma damselfly species to evaluate demographic contributions of three mechanisms affecting different fitness components across the life cycle: the effect of resource competition on individual growth rate, predation shaping mortality rates, and mating harassment determining fecundity. We then used a demographic model that incorporates carry-over effects between life stages to decompose the relative effect of each fitness component generating frequency-dependent population growth. This decomposition showed that fitness components combined to increase population growth rates for one species when rare, but they combined to decrease population growth rates for the other species when rare, leading to predicted exclusion in most lakes. Because interactions between fitness components within and between life stages vary among populations, these results show that local coexistence is population specific. Moreover, we show that multiple mechanisms do not necessarily increase competitor coexistence, as they can also combine to yield exclusion. Identifying coexistence mechanisms in other systems will require greater focus on determining contributions of different fitness components across the life cycle shaping competitor coexistence in a way that captures the potential for population-level variation.

Environmental Conditions during Development Affect Sexual Selection through Trait-Fitness Relationships.

AbstractSexual selection can be shaped by spatial variation in environmental features among populations. Differences in sexual selection among populations generated through the effects of the environment could be shaped via four paths: differences in mean absolute fitness, differences in the means or variances of phenotypes, or differences in the absolute fitness-trait function relationship. Because sexual selection occurs only during the adult life stage, most studies have focused on identifying environmental features that influence these metrics of fitness and trait distributions among adults. However, these adult features could also be affected by environmental factors experienced in early life stages that then shape the trajectory for sexual selection during the adult life stage. Here we investigated how among-population variation in environmental conditions during the juvenile (larval) stage of two species of Enallagma damselflies shapes sexual selection on male body size. We found that environmental factors related to predation pressures, lake primary productivity, and habitat availability play a role in shaping spatial variation in sexual selection. This acts mainly through how the environment affects absolute fitness-body size associations, not spatial variation in mean fitness or body size means and variances. These results demonstrate that the underpinnings of sexual selection in the wild can arise from environmental conditions during prereproductive life stages.

Parasitism shapes selection by drastically reducing host fitness and increasing host fitness variation.

Determining the effects of parasites on host reproduction is key to understanding how parasites affect the underpinnings of selection on hosts. Although infection is expected to be costly, reducing mean fitness, infection could also increase variation in fitness costs among hosts, both of which determine the potential for selection on hosts. To test these ideas, we used a phylogenetically informed meta-analysis of 118 studies to examine how changes in the mean and variance in the outcome of reproduction differed between parasitized and non-parasitized hosts. We found that parasites had severe negative effects on mean fitness, with parasitized hosts suffering reductions in fecundity, viability and mating success. Parasite infection also increased variance in reproduction, particularly fecundity and offspring viability. Surprisingly, parasites had similar effects on viability when either the male or female was parasitized. These results not only provide the first synthetic, comparative, and quantitative summary of the strong deleterious effects of parasites on host reproductive fitness, but also reveal a consistent role for parasites in shaping the opportunity for selection.

Bovine tuberculosis disturbs parasite functional trait composition in African buffalo.

Novel parasites can have wide-ranging impacts, not only on host populations, but also on the resident parasite community. Historically, impacts of novel parasites have been assessed by examining pairwise interactions between parasite species. However, parasite communities are complex networks of interacting species. Here we used multivariate taxonomic and trait-based approaches to determine how parasite community composition changed when African buffalo (Syncerus caffer) acquired an emerging disease, bovine tuberculosis (BTB). Both taxonomic and functional parasite richness increased significantly in animals that acquired BTB than in those that did not. Thus, the presence of BTB seems to catalyze extraordinary shifts in community composition. There were no differences in overall parasite taxonomic composition between infected and uninfected individuals, however. The trait-based analysis revealed an increase in direct-transmitted, quickly replicating parasites following BTB infection. This study demonstrates that trait-based approaches provide insight into parasite community dynamics in the context of emerging infections.

Predators weaken prey intraspecific competition through phenotypic selection.

Predators have a key role shaping competitor dynamics in food webs. Perhaps the most obvious way this occurs is when predators reduce competitor densities. However, consumption could also generate phenotypic selection on prey that determines the strength of competition, thus coupling consumptive and trait-based effects of predators. In a mesocosm experiment simulating fish predation on damselflies, we found that selection against high damselfly activity rates - a phenotype mediating predation and competition - weakened the strength of density dependence in damselfly growth rates. A field experiment corroborated this finding and showed that increasing damselfly densities in lakes with high fish densities had limited effects on damselfly growth rates but generated a precipitous growth rate decline where fish densities were lower - a pattern expected because of spatial variation in selection imposed by predation. These results suggest that accounting for both consumption and selection is necessary to determine how predators regulate prey competitive interactions.

Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed-dispersing ants.

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy-fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.

No evidence that warmer temperatures are associated with selection for smaller body sizes.

Reductions in animal body size over recent decades are often interpreted as an adaptive evolutionary response to climate warming. However, for reductions in size to reflect adaptive evolution, directional selection on body size within populations must have become negative, or where already negative, to have become more so, as temperatures increased. To test this hypothesis, we performed traditional and phylogenetic meta-analyses of the association between annual estimates of directional selection on body size from wild populations and annual mean temperatures from 39 longitudinal studies. We found no evidence that warmer environments were associated with selection for smaller size. Instead, selection consistently favoured larger individuals, and was invariant to temperature. These patterns were similar in ectotherms and endotherms. An analysis using year rather than temperature revealed similar patterns, suggesting no evidence that selection has changed over time, and also indicating that the lack of association with annual temperature was not an artefact of choosing an erroneous time window for aggregating the temperature data. Although phenotypic trends in size will be driven by a combination of genetic and environmental factors, our results suggest little evidence for a necessary ingredient-negative directional selection-for declines in body size to be considered an adaptive evolutionary response to changing selection pressures.

Disentangling ecologically equivalent from neutral species: The mechanisms of population regulation matter.

The neutral theory of biodiversity explored the structure of a community of ecologically equivalent species. Such species are expected to display community drift dynamics analogous to neutral alleles undergoing genetic drift. While entire communities of species are not ecologically equivalent, recent field experiments have documented the existence of guilds of such neutral species embedded in real food webs. What demographic outcomes of the interactions within and between species in these guilds are expected to produce ecological drift versus coexistence remains unclear. To address this issue, and guide empirical testing, we consider models of a guild of ecologically equivalent competitors feeding on a single resource to explore when community drift should manifest. We show that community drift dynamics only emerge when the density-dependent effects of each species on itself are identical to its density-dependent effects on every other guild member. In contrast, if each guild member directly limits itself more than it limits the abundance of other guild members, all species in the guild are coexisting, even though they all are ecologically equivalent with respect to their interactions with species outside the guild (i.e. resources, predators, mutualists). Hence, considering only interspecific ecological differences generating density dependence, and not fully accounting for the preponderance of mechanisms causing intraspecific density dependence, will provide an incomplete picture for segregating between neutrality and coexistence. We also identify critical experiments necessary to disentangle guilds of ecologically equivalent species from those experiencing ecological drift, as well as provide an overview of ways of incorporating a mechanistic basis into studies of species coexistence and neutrality. Identifying these characteristics, and the mechanistic basis underlying community structure, is not merely an exercise in clarifying the semantics of coexistence and neutral theories, but rather reflects key differences that must exist among community members in order to determine how and why communities are structured.

A framework for linking competitor ecological differences to coexistence.

Not all ecological differences among competing species affect their ability to locally coexist. Rather, the differences that promote stable coexistence can be those which cause each species to experience stronger intraspecific than interspecific competition. Recent approaches have established how to detect the demographic signature of these competitive effects, but alone they cannot elucidate the ecological differences among species that yield these patterns. Here, we present a unifying experimental and observational framework that identifies potential ecological differences among species shaping their responses to intra- and interspecific competition. We first describe a conceptual model establishing why the strength of intra- and interspecific competitive interactions should vary along environmental gradients related to species ecological differences. We then show how to apply the framework using Enallagma damselflies, a diverse group of predatory aquatic insects. To determine how species responded to intra- and interspecific competition along environmental gradients, we experimentally manipulated the relative abundances of three species and replicated this across five lakes which varied in environmental conditions affecting larval damselfly per capita growth and mortality rates-key vital rates regulating their populations. Results suggest Enallagma are ecologically differentiated in ways that in some communities can result in intraspecific competition exceeding interspecific competition. However, in many cases the opposite was true, or the effects of intra- and interspecific competition were equivalent via growth and mortality responses. Moreover, these effects tended to be weak and asymmetrical among competitors, which suggests that differential responses of larval growth and mortality to intra- and interspecific competition may not contribute strongly to the maintenance of Enallagma diversity. Different environmental factors appear to shape these demographic responses to competition, providing insight into the ecological mechanisms regulating damselfly assemblages. This framework can be broadly applied to identify the ecological differences among species that may promote coexistence, advancing knowledge of the mechanisms underlying coexistence and overcoming some limitations of purely phenomenological approaches.

Tipping Points in Resource Abundance Drive Irreversible Changes in Community Structure.

Global climate change has made what were seemingly extraordinary environmental conditions, such as prolonged droughts, commonplace. One consequence of extreme environmental change is concomitant changes in resource abundance. How will such extreme resource changes impact biodiversity? We developed a trait-based consumer-resource model to examine how resource abundance affects the potential for adaptive evolution and coexistence among competitors. We found that moderate changes in resource abundance have little effect on trait evolution. However, when resource scarcities were sufficiently extreme, a critical transition-a tipping point-occurred, which caused consumer traits to diverge and restructured the community in a way that outlasted the scarcity. Therefore, even though traits can evolve in response to minor resource fluctuations, large environmental shifts may be necessary for producing long-lasting impacts on community structure. These results may also help to illuminate patterns of stasis frequently observed in nature, despite the considerable evidence demonstrating rapid evolutionary change.

Female mate preferences on high-dimensional shape variation for male species recognition traits.

Females in many animal species must discriminate between conspecific and heterospecific males when choosing mates. Such mating preferences that discriminate against heterospecifics may inadvertently also affect the mating success of conspecific males, particularly those with more extreme phenotypes. From this expectation, we hypothesized that female mate choice should cause Enallagma females (Odonata: Coenagrionidae) to discriminate against conspecific males with more extreme phenotypes of the claspers males use to grasp females while mating - the main feature of species mate recognition in these species. To test this, we compared cerci sizes and shapes between males that were captured while mating with females to males that were captured at the same time but not mating in three Enallagma species. In contrast to our hypothesis, we found only one of forty comparisons of shape variation that was consistent with females discriminating against males with more extreme cerci shapes. Instead, differences in cerci shape between mating and single males suggested that females displayed directional preferences on 1-4 aspects of cerci shape in two of the species in our samples. These results suggest that whereas some directional biases in mating based on cerci shape occur, the intraspecific phenotypic variation in male cerci size and shape is likely not large enough for females to express any significant incidental discrimination among conspecifics with more extreme shapes.

Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events.

Mass mortality events (MMEs) are rapidly occurring catastrophic demographic events that punctuate background mortality levels. Individual MMEs are staggering in their observed magnitude: removing more than 90% of a population, resulting in the death of more than a billion individuals, or producing 700 million tons of dead biomass in a single event. Despite extensive documentation of individual MMEs, we have no understanding of the major features characterizing the occurrence and magnitude of MMEs, their causes, or trends through time. Thus, no framework exists for contextualizing MMEs in the wake of ongoing global and regional perturbations to natural systems. Here we present an analysis of 727 published MMEs from across the globe, affecting 2,407 animal populations. We show that the magnitude of MMEs has been intensifying for birds, fishes, and marine invertebrates; invariant for mammals; and decreasing for reptiles and amphibians. These shifts in magnitude proved robust when we accounted for an increase in the occurrence of MMEs since 1940. However, it remains unclear whether the increase in the occurrence of MMEs represents a true pattern or simply a perceived increase. Regardless, the increase in MMEs appears to be associated with a rise in disease emergence, biotoxicity, and events produced by multiple interacting stressors, yet temporal trends in MME causes varied among taxa and may be associated with increased detectability. In addition, MMEs with the largest magnitudes were those that resulted from multiple stressors, starvation, and disease. These results advance our understanding of rare demographic processes and their relationship to global and regional perturbations to natural systems.

What Are the Environmental Determinants of Phenotypic Selection? A Meta-analysis of Experimental Studies.

Although many selection estimates have been published, the environmental factors that cause selection to vary in space and time have rarely been identified. One way to identify these factors is by experimentally manipulating the environment and measuring selection in each treatment. We compiled and analyzed selection estimates from experimental studies. First, we tested whether the effect of manipulating the environment on selection gradients depends on taxon, trait type, or fitness component. We found that the effect of manipulating the environment was larger when selection was measured on life-history traits or via survival. Second, we tested two predictions about the environmental factors that cause variation in selection. We found support for the prediction that variation in selection is more likely to be caused by environmental factors that have a large effect on mean fitness but not for the prediction that variation is more likely to be caused by biotic factors. Third, we compared selection gradients from experimental and observational studies. We found that selection varied more among treatments in experimental studies than among spatial and temporal replicates in observational studies, suggesting that experimental studies can detect relationships between environmental factors and selection that would not be apparent in observational studies.

Experimental Evidence for an Eco-Evolutionary Coupling between Local Adaptation and Intraspecific Competition.

Determining how adaptive evolution can be coupled to ecological processes is key for developing a more integrative understanding of the demographic factors that regulate populations. Intraspecific competition is an especially important ecological process because it generates negative density dependence in demographic rates. Although ecological factors are most often investigated to determine the strength of density dependence, evolutionary processes such as local adaptation could also feed back to shape variation in the strength of density dependence among populations. Using an experimental approach with damselflies, a predaceous aquatic insect, we find evidence that both density-dependent intraspecific competition and local adaptation can reduce per capita growth rates. In some cases, the effects of local adaptation on reducing per capita growth rates exceeded the ecological competitive effects of a doubling of density. However, we also found that these ecological and evolutionary properties of populations are coupled, and we offer two interpretations of the causes underlying this pattern: (1) the strength of density-dependent competition depends on the extent of local adaptation, or (2) the extent of local adaptation is shaped by the strength of density-dependent competition. Regardless of the underlying causal pathway, these results show how eco-evolutionary dynamics can affect a key demographic process regulating populations.

The spatial patterns of directional phenotypic selection.

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta-analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.

Differences in the temporal dynamics of phenotypic selection among fitness components in the wild.

The balance of selection acting through different fitness components (e.g. fecundity, mating success, survival) determines the potential tempo and trajectory of adaptive evolution. Yet the extent to which the temporal dynamics of phenotypic selection may vary among fitness components is poorly understood. Here, we compiled a database of 3978 linear selection coefficients from temporally replicated studies of selection in wild populations to address this question. Across studies, we find that multi-year selection through mating success and fecundity is stronger than selection through survival, but varies less in direction. We also report that selection through mating success varies more in long-term average strength than selection through either survival or fecundity. The consistency in direction and stronger long-term average strength of selection through mating success and fecundity suggests that selection through these fitness components should cause more persistent directional evolution relative to selection through survival. Similar patterns were apparent for the subset of studies that evaluated the temporal dynamics of selection on traits simultaneously using several different fitness components, but few such studies exist. Taken together, these results reveal key differences in the temporal dynamics of selection acting through different fitness components, but they also reveal important limitations in our understanding of how selection drives adaptive evolution.