Time-dependent interaction modification generated from plant-soil feedback.

Pairwise interactions between species can be modified by other community members, leading to emergent dynamics contingent on community composition. Despite the prevalence of such higher-order interactions, little is known about how they are linked to the timing and order of species' arrival. We generate population dynamics from a mechanistic plant-soil feedback model, then apply a general theoretical framework to show that the modification of a pairwise interaction by a third plant depends on its germination phenology. These time-dependent interaction modifications emerge from concurrent changes in plant and microbe populations and are strengthened by higher overlap between plants' associated microbiomes. The interaction between this overlap and the specificity of microbiomes further determines plant coexistence. Our framework is widely applicable to mechanisms in other systems from which similar time-dependent interaction modifications can emerge, highlighting the need to integrate temporal shifts of species interactions to predict the emergent dynamics of natural communities.

Predation and competition drive trait diversity across space and time.

Competition should play a key role in shaping community assembly and thereby local and regional biodiversity patterns. However, identifying its relative importance and effects in natural communities is challenging because theory suggests that competition can lead to different and even opposing patterns depending on the underlying mechanisms. Here, we have taken a different approach: rather than attempting to indirectly infer competition from diversity patterns, we compared trait diversity patterns in odonate (dragonfly and damselfly) communities across different spatial and temporal scales along a natural competition-predation gradient. At the local scale (within a community), we found that trait diversity increased with the size of top predators (from invertebrates to fish). This relationship is consistent with differences in taxonomic diversity, suggesting that competition reduces local trait diversity through competitive exclusion. Spatial (across communities) and temporal (within communities over time) trait variation peaked in communities with intermediate predators indicating that both high levels of competition or predation select for trait convergence of communities. This indicates that competition acts as a deterministic force that reduces trait diversity at the local, regional, and temporal scales, which contrasts with patterns at the taxonomic level. Overall, results from this natural experiment reveal how competition and predation interact to shape biodiversity patterns in natural communities across spatial and temporal scales and provide new insights into the underlying mechanisms.

Stage-mediated priority effects and season lengths shape long-term competition dynamics.

The relative arrival time of species can affect their interactions and thus determine which species persist in a community. Although this phenomenon, called priority effect, is widespread in natural communities, it is unclear how it depends on the length of growing season. Using a seasonal stage-structured model, we show that differences in stages of interacting species could generate priority effects by altering the strength of stabilizing and equalizing coexistence mechanisms, changing outcomes between exclusion, coexistence and positive frequency dependence. However, these priority effects are strongest in systems with just one or a few generations per season and diminish in systems where many overlapping generations per season dilute the importance of stage-specific interactions. Our model reveals a novel link between the number of generations in a season and the consequences of priority effects, suggesting that consequences of phenological shifts driven by climate change should depend on specific life histories of organisms.

Bridging theory and experiments of priority effects.

Priority effects play a key role in structuring natural communities, but considerable confusion remains about how they affect different ecological systems. Synthesizing previous studies, we show that this confusion arises because the mechanisms driving priority and the temporal scale at which they operate differ among studies, leading to divergent outcomes in species interactions and biodiversity patterns. We suggest grouping priority effects into two functional categories based on their mechanisms: frequency-dependent priority effects that arise from positive frequency dependence, and trait-dependent priority effects that arise from time-dependent changes in interacting traits. Through easy quantification of these categories from experiments, we can construct community models representing diverse biological mechanisms and interactions with priority effects, therefore better predicting their consequences across ecosystems.

Priority Effects Determine How Dispersal Affects Biodiversity in Seasonal Metacommunities.

AbstractThe arrival order of species frequently determines the outcome of their interactions. This phenomenon, called the priority effect, is ubiquitous in nature and determines local community structure, but we know surprisingly little about how it influences biodiversity across different spatial scales. Here, we use a seasonal metacommunity model to show that biodiversity patterns and the homogenizing effect of high dispersal depend on the specific mechanisms underlying priority effects. When priority effects are driven only by positive frequency dependence, dispersal-diversity relationships are sensitive to initial conditions but generally show a hump-shaped relationship: biodiversity declines when dispersal rates become high and allow the dominant competitor to exclude other species across patches. When spatiotemporal variation in phenological differences alters species' interaction strengths (trait-dependent priority effects), local, regional, and temporal diversity are surprisingly insensitive to variation in dispersal, regardless of the initial numeric advantage. Thus, trait-dependent priority effects can strongly reduce the effect of dispersal on biodiversity, preventing the homogenization of metacommunities. Our results suggest an alternative mechanism that maintains local and regional diversity without environmental heterogeneity, highlighting that accounting for the mechanisms underlying priority effects is fundamental to understanding patterns of biodiversity.

Exploring Conditions That Strengthen or Weaken the Ecological and Evolutionary Consequences of Phenological Synchrony.

AbstractClimate change-driven phenological shifts alter the temporal distributions of natural populations and communities, but we have little understanding of how these shifts affect natural populations. Using agent-based models, we show that the interaction of within-population synchrony (individual variation in timing) and timing of interspecific interactions shapes ecological and evolutionary dynamics of populations within a seasonal cycle. Low-synchrony populations had lower survival and biomass but relatively stronger individuals. These effects were surprisingly robust and did not require size-based competitive asymmetries. However, reducing population synchrony could either negatively or positively affect population demography depending on whether the phenology of the focal species was advanced or delayed relative to its competitor. Furthermore, selection for earlier hatching increased when the interspecific competitor arrived earlier and when population synchrony was high. These results emphasize the importance of variation in the phenology of individuals within populations to better understand species interactions and predict ecological and evolutionary outcomes of phenological shifts.

Climate warming promotes pesticide resistance through expanding overwintering range of a global pest.

Climate change has the potential to change the distribution of pests globally and their resistance to pesticides, thereby threatening global food security in the 21st century. However, predicting where these changes occur and how they will influence current pest control efforts is a challenge. Using experimentally parameterised and field-tested models, we show that climate change over the past 50 years increased the overwintering range of a global agricultural insect pest, the diamondback moth (Plutella xylostella), by ~2.4 million km2 worldwide. Our analysis of global data sets revealed that pesticide resistance levels are linked to the species' overwintering range: mean pesticide resistance was 158 times higher in overwintering sites compared to sites with only seasonal occurrence. By facilitating local persistence all year round, climate change can promote and expand pesticide resistance of this destructive species globally. These ecological and evolutionary changes would severely impede effectiveness of current pest control efforts and potentially cause large economic losses.

Developmental Change in Predators Drives Different Community Configurations.

AbstractTheoreticians who first observed alternative stable states in simple ecological models warned of grave implications for unexpected and irreversible collapses of natural systems (i.e., regime shifts). Recent ecosystem-level shifts engendering considerable economic losses have validated this concern, positioning bistability at the vanguard of coupled human-environment systems management. While the perturbations that induce regime shifts are known, the ecological forces that uphold alternative stable states are often unresolved or complex and system specific. Thus, the search continues for general mechanisms that can produce alternative stable states under realistic conditions. Integrating model predictions with long-term zooplankton community experiments, we show that the core feature of ontogenetic development, food-dependent maturation, enables a single community to reach different configurations within the same constant environment. In one configuration, predators regulate prey to foster coexistence, while in the other, prey counterintuitively exclude their predators via maturation-limiting competition. The concordance of these findings with the unique outcome and underlying mechanism of a general model provides empirical evidence that developmental change, a fundamental property of life, can support bistability of natural systems.

Ontogenetic diversity buffers communities against consequences of species loss.

Biodiversity can be measured at multiple organizational scales. While traditional studies have focused at taxonomic diversity, recent studies have emphasized the ecological importance of diversity within populations. However, it is unclear how these different scales of diversity interact to determine the consequence of species loss. Here we asked how predator diversity and presence of ontogenetic diversity within predator populations influences community structure. Ontogenetic diversity arises from shifts in the traits and ecology of individuals during ontogeny and it is one of the biggest sources of intraspecific diversity. However, whether it dampens or strengthens the negative consequences of with species loss is poorly understood. To study the interaction of species diversity and ontogenetic diversity, we experimentally manipulated predator species diversity and diversity of developmental stages within focal predator species and analysed their joint effect on predator and prey survival, biomass and prey community structure in experimental pond systems. While individual effects of ontogenetic diversity were often species specific, losing predator species from the community often had a much smaller or no effect on prey survival, biomass or community structure when all predator populations had high ontogenetic diversity. Thus, ontogenetic diversity within populations buffered against some of the consequences of biodiversity loss at higher organizational levels. Because the experiment controlled mean per capita size and biomass across structured versus unstructured populations, this pattern was not driven by differences in biomass of predators. Instead, results suggest that effects were driven by changes in the functional roles and indirect interactions across and within species. This indicates that even if all environmental conditions are similar, differences in the intrinsic structure of populations can modify the consequences of biodiversity loss. Together, these results revealed the importance of ontogenetic diversity within species for strengthening the resilience of natural communities to consequences of biodiversity loss and emphasize the need to integrate biodiversity patterns across organizational scales.

Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations.

Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts.

How parasite interaction strategies alter virulence evolution in multi-parasite communities.

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within-host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite-induced host mortality). Yet we still know little about how within-host interactions affect the evolution of parasite virulence in multi-parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within-host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.

Shifts in phenological mean and synchrony interact to shape competitive outcomes.

Climate change-induced phenological shifts are ubiquitous and have the potential to disrupt natural communities by changing the timing of species interactions. Shifts in first and/or mean phenological date are well documented, but recent studies indicate that shifts in synchrony (individual variation around these metrics) can be just as common. However, we know little about how both types of phenological shifts interact to affect species interactions and communities. Here, we experimentally manipulated the hatching phenologies of two competing species of larval amphibians to address this conceptual gap. Specifically, we manipulated the relative mean hatching time (early, same, or late relative to competitor) and population synchrony (high, medium, or low levels of variation around the mean) in a full 3 × 3 factorial design to measure independent and interactive effects of phenological mean and population phenological synchrony on competitive outcomes. Our results indicate that phenological synchrony within a population strongly influences intraspecific competition by changing the density of individuals and relative strength of early- vs. late-arriving individuals. Individuals from high-synchrony populations competed symmetrically, whereas individuals from low-synchrony populations competed asymmetrically. At the community scale, shifts in population phenological synchrony interact with shifts in phenological mean to affect key demographic rates (survival, biomass export, per capita mass, and emergence timing) strongly. Furthermore, changes in mean timing of species interactions altered phenological synchrony within a population at the next life stage, and phenological synchrony at one life stage altered the mean timing of the next life stage. Thus, shifts in phenological synchrony within populations cannot only alter species interactions, but species interactions in turn can also drive shifts in phenology.

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.

Opportunities for behavioral rescue under rapid environmental change.

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

The role of seasonal timing and phenological shifts for species coexistence.

Shifts in the phenologies of coexistence species are altering the temporal structure of natural communities worldwide. However, predicting how these changes affect the structure and long-term dynamics of natural communities is challenging because phenology and coexistence theory have largely proceeded independently. Here, I propose a conceptual framework that incorporates seasonal timing of species interactions into a well-studied competition model to examine how changes in phenologies influence long-term dynamics of natural communities. Using this framework I demonstrate that persistence and coexistence conditions strongly depend on the difference in species' mean phenologies and how this difference varies across years. Consequently, shifts in mean and interannual variation in relative phenologies of species can fundamentally alter the outcome of interactions and the potential for persistence and coexistence of competing species. These effects can be predicted by how per-capita effects scale with differences in species' phenologies. I outline how this approach can be parameterized with empirical systems and discuss how it fits within the context of current coexistence theory. Overall, this synthesis reveals that phenology of species interactions can play a crucial yet currently understudied role in driving coexistence and biodiversity patterns in natural systems and determine how species will respond to future climate change.

Within-Host Priority Effects Systematically Alter Pathogen Coexistence.

Coinfection of host populations alters pathogen prevalence, host mortality, and pathogen evolution. Because pathogens compete for limiting resources, whether multiple pathogens can coexist in a host population can depend on their within-host interactions, which, in turn, can depend on the order in which pathogens infect hosts (within-host priority effects). However, the consequences of within-host priority effects for pathogen coexistence have not been tested. Using laboratory studies with a coinfected zooplankton system, we found that pathogens had increased fitness in coinfected hosts when they were the second pathogen to infect a host, compared to when they were the first pathogen to infect a host. With these results, we parameterized a pathogen coexistence model with priority effects, finding that pathogen coexistence (1) decreased when priority effects increased the fitness of the first pathogen to arrive in coinfected hosts and (2) increased when priority effects increased the fitness of the second pathogen to arrive in coinfected hosts. We also identified the natural conditions under which we expect within-host priority effects to foster coexistence in our system. These outcomes were the result of positive or negative frequency dependence created by feedback loops between pathogen prevalence and infection order in coinfected hosts. This suggests that priority effects can systematically alter conditions for pathogen coexistence in host populations, thereby changing pathogen community structure and potentially altering host mortality and pathogen evolution via emergent processes.

Prey Limitation Drives Variation in Allometric Scaling of Predator-Prey Interactions.

Ecologists have long searched for a universal size-scaling constant that governs trophic interactions. Although this is an appealing theoretical concept, predator-prey size ratios (PPSRs) vary strikingly across and within natural food webs, meaning that predators deviate from their optimal prey size by consuming relatively larger or smaller prey. Here we suggest that this unexpected variation in allometric scaling of trophic interactions can be predicted by gradients of prey limitation consistent with predictions from optimal foraging theory. We analyzed >6,000 trophic interactions of 52 populations from four tropical frog species along a gradient of prey limitation. The mean of PPSR and its variance differed up to two orders of magnitude across and within food webs. Importantly, as prey availability decreased across food webs, PPSR and its variance became more size dependent. Thus, trophic interactions did not follow a fixed allometric scaling but changed predictably with the strength of prey limitation. Our results emphasize the importance of ecological contexts in arranging food webs and the need to incorporate ecological drivers of PPSR and its variance in food web and community models.

Resource limitation alters effects of phenological shifts on inter-specific competition.

Phenological shifts can alter the relative arrival time of competing species in natural communities, but predicting the consequences for species interactions and community dynamics is a major challenge. Here we show that differences in relative arrival time can lead to predictable priority effects that alter the outcome of competitive interactions. By experimentally manipulating the relative arrival time of two competing tadpole species across a resource gradient, we found that delaying relative arrival of a species reduced the interaction asymmetry between species and could even reverse competitive dominance. However, the strength of these priority effects was contingent on the abundance of the shared resource. Priority effects were generally weak when resources were limited, but increased at higher resource levels. Importantly, this context dependency could be explained by a shift in per capita interaction strength driven by a shift in relative body sizes of competitors. These results shed new light into the mechanisms that drive variation in priority effects and help predict consequences of phenological shifts across different environments.

Drivers of individual niche variation in coexisting species.

Although neglected by classic niche theory, individual variation is now recognized as a prevalent phenomenon in nature with evolutionary and ecological relevance. Recent theory suggests that differences in individual variation across competitors can affect species coexistence and community patterns. However, the degree of individual variation is flexible across wild populations and we still know little about the ecological drivers of this variation across populations of single species and, especially, across coexisting species. Here, we aimed to (a) elucidate the major drivers of individual niche variation in natural communities and (b) to determine how consistent this variation is across coexisting species and communities. We analysed natural patterns of individual-level niche variation in four species of coexisting generalist frogs across a wide range of tropical communities. Specifically, we used gut contents and stable isotopes (δ13 C and δ15 N) from frog species and their prey to quantify individual niche specialization. Then, we combined data on local community structure, availability of prey, phylogenetic relationships and predator-prey size models to test how this variation is related to four ecological factors which are predicted to be key drivers of individual specialization: intraspecific competition, interspecific competition, ecological opportunity (i.e., diversity of resources) and predation. We found that the degree of individual trophic specialization varied by up to ninefold across populations within the same species. This sizable variation in trophic specialization across populations was at least partially explained by gradients of density of competitors (both conspecifics and heterospecifics) and intraguild predation. However, the specific relationships between individual specialization and these ecological gradients were strongly species-specific. As consequences, the identity of the species with more individual variation changed among sites and there was typically no spatial correlation in the degree of individual specialization across coexisting species. Our results show that individual niche specialization within and across species can be strongly context-dependent and that hierarchies of individual variation among coexisting species are not necessarily consistent across communities. Recent theory suggests that this pattern could lead to concurrent changes in competitive interactions across sites and thereby could play a key role in species coexistence at the landscape level. Our results suggest that individual variation across and within coexisting species has the potential to affect not only species coexistence at local communities, but also regional diversity patterns.