Competitive history shapes rapid evolution in a seasonal climate.

Eco-evolutionary dynamics will play a critical role in determining species' fates as climatic conditions change. Unfortunately, we have little understanding of how rapid evolutionary responses to climate play out when species are embedded in the competitive communities that they inhabit in nature. We tested the effects of rapid evolution in response to interspecific competition on subsequent ecological and evolutionary trajectories in a seasonally changing climate using a field-based evolution experiment with Drosophila melanogaster Populations of D. melanogaster were either exposed, or not exposed, to interspecific competition with an invasive competitor, Zaprionus indianus, over the summer. We then quantified these populations' ecological trajectories (abundances) and evolutionary trajectories (heritable phenotypic change) when exposed to a cooling fall climate. We found that competition with Z. indianus in the summer affected the subsequent evolutionary trajectory of D. melanogaster populations in the fall, after all interspecific competition had ceased. Specifically, flies with a history of interspecific competition evolved under fall conditions to be larger and have lower cold fecundity and faster development than flies without a history of interspecific competition. Surprisingly, this divergent fall evolutionary trajectory occurred in the absence of any detectible effect of the summer competitive environment on phenotypic evolution over the summer or population dynamics in the fall. This study demonstrates that competitive interactions can leave a legacy that shapes evolutionary responses to climate even after competition has ceased, and more broadly, that evolution in response to one selective pressure can fundamentally alter evolution in response to subsequent agents of selection.

Rapid evolution of life-history traits in response to warming, predation and competition: A meta-analysis.

Although studies quantifying evolutionary change in response to the selective pressures that organisms face in the wild have demonstrated that organisms can evolve rapidly, we lack a systematic assessment of the frequency, magnitude and direction of rapid evolutionary change across taxa. To address this gap, we conducted a meta-analysis of 58 studies that document the effects of warming, predation or competition on the evolution of body size, development rate or fecundity in natural or experimental animal populations. We tested whether there was a consistent effect of any selective agent on any trait, whether the direction of these effects align with theoretical predictions, and whether the three agents select in opposing directions on any trait. Overall, we found weak effects of all three selective agents on trait evolution: none of our nine traits by selective agent combinations had an overall effect that differed from zero, only 31% of studies had a significant within-study effect, and attributes of the included studies generally did not account for between-study variation in results. One notable exception was that predation targeting adults consistently resulted in the evolution of smaller prey body size. We discuss potential causes of these generally weak responses and consider how our results inform the ongoing development of eco-evolutionary research.

Applying modern coexistence theory to priority effects.

Modern coexistence theory is increasingly used to explain how differences between competing species lead to coexistence versus competitive exclusion. Although research testing this theory has focused on deterministic cases of competitive exclusion, in which the same species always wins, mounting evidence suggests that competitive exclusion is often historically contingent, such that whichever species happens to arrive first excludes the other. Coexistence theory predicts that historically contingent exclusion, known as priority effects, will occur when large destabilizing differences (positive frequency-dependent growth rates of competitors), combined with small fitness differences (differences in competitors' intrinsic growth rates and sensitivity to competition), create conditions under which neither species can invade an established population of its competitor. Here we extend the empirical application of modern coexistence theory to determine the conditions that promote priority effects. We conducted pairwise invasion tests with four strains of nectar-colonizing yeasts to determine how the destabilizing and fitness differences that drive priority effects are altered by two abiotic factors characterizing the nectar environment: sugar concentration and pH. We found that higher sugar concentrations increased the likelihood of priority effects by reducing fitness differences between competing species. In contrast, higher pH did not change the likelihood of priority effects, but instead made competition more neutral by bringing both fitness differences and destabilizing differences closer to zero. This study demonstrates how the empirical partitioning of priority effects into fitness and destabilizing components can elucidate the pathways through which environmental conditions shape competitive interactions.

Temperature-Dependent Species Interactions Shape Priority Effects and the Persistence of Unequal Competitors.

The order of species arrival at a site can determine the outcome of competitive interactions when early arrivers alter the environment or deplete shared resources. These priority effects are predicted to be stronger at high temperatures, as higher vital rates caused by warming allow early arrivers to more rapidly impact a shared environment. We tested this prediction using a pair of congeneric aphid species that specialize on milkweed plants. We manipulated temperature and arrival order of the two aphid species and measured aphid population dynamics and milkweed survival and defensive traits. We found that warming increased the impact of aphids on the quantity and quality of milkweed, which amplified the importance of priority effects by increasing the competitive exclusion of the inferior competitor when it arrived late. Warming also enhanced interspecific differences in dispersal, which could alter relative arrival times at a regional scale. Our experiment provides a first link between temperature-dependent trophic interactions, priority effects, and dispersal. This study suggests that the indirect and cascading effects of temperature observed here may be important determinants of diversity in the temporally and spatially complex landscapes that characterize ecological communities.

Predators modify biogeographic constraints on species distributions in an insect metacommunity.

Theory describing the positive effects of patch size and connectivity on diversity in fragmented systems has stimulated a large body of empirical work, yet predicting when and how local species interactions mediate these responses remains challenging. We used insects that specialize on milkweed plants as a model metacommunity to investigate how local predation alters the effects of biogeographic constraints on species distributions. Species-specific dispersal ability and susceptibility to predation were used to predict when patch size and connectivity should shape species distributions, and when these should be modified by local predator densities. We surveyed specialist herbivores and their predators in milkweed patches in two matrix types, a forest and an old field. Predator-resistant species showed the predicted direct positive effects of patch size and connectivity on occupancy rates. For predator-susceptible species, predators consistently altered the impact of biogeographic constraints, rather than acting independently. Finally, differences between matrix types in species' responses and overall occupancy rates indicate a potential role of the inter-patch environment in mediating the joint effects of predators and spatial drivers. Together, these results highlight the importance of local top-down pressure in mediating classic biogeographic relationships, and demonstrate how species-specific responses to local and regional constraints can be used to predict these effects.

Multi-scale responses to warming in an experimental insect metacommunity.

In metacommunities, diversity is the product of species interactions at the local scale and dispersal between habitat patches at the regional scale. Although warming can alter both species interactions and dispersal, the combined effects of warming on these two processes remains uncertain. To determine the independent and interactive effects of warming-induced changes to local species interactions and dispersal, we constructed experimental metacommunities consisting of enclosed milkweed patches seeded with five herbivorous milkweed specialist insect species. We treated metacommunities with two levels of warming (unwarmed and warmed) and three levels of connectivity (isolated, low connectivity, high connectivity). Based on metabolic theory, we predicted that if plant resources were limited, warming would accelerate resource drawdown, causing local insect declines and increasing both insect dispersal and the importance of connectivity to neighboring patches for insect persistence. Conversely, given abundant resources, warming could have positive local effects on insects, and the risk of traversing a corridor to reach a neighboring patch could outweigh the benefits of additional resources. We found support for the latter scenario. Neither resource drawdown nor the weak insect-insect associations in our system were affected by warming, and most insect species did better locally in warmed conditions and had dispersal responses that were unchanged or indirectly affected by warming. Dispersal across the matrix posed a species-specific risk that led to declines in two species in connected metacommunities. Combined, this scaled up to cause an interactive effect of warming and connectivity on diversity, with unwarmed metacommunities with low connectivity incurring the most rapid declines in diversity. Overall, this study demonstrates the importance of integrating the complex outcomes of species interactions and spatial structure in understanding community response to climate change.

An invasive herbivore structures plant competitive dynamics.

Species interactions are central to our understanding of ecological communities, but may change rapidly with the introduction of invasive species. Invasive species can alter species interactions and community dynamics directly by having larger detrimental effects on some species than others, or indirectly by changing the ways in which native species compete among themselves. We tested the direct and indirect effects of an invasive aphid herbivore on a native aphid species and two host milkweed species. The invasive aphid caused a 10-fold decrease in native aphid populations, and a 30% increase in plant mortality (direct effects). The invasive aphid also increased the strength of interspecific competition between the two native plant hosts (indirect effects). By investigating the role that indirect effects play in shaping species interactions in native communities, our study highlights an understudied component of species invasions.

The Invasion Criterion: A Common Currency for Ecological Research.

According to the invasion criterion, stable coexistence requires that all species in a community increase in abundance when rare, which occurs when stabilizing mechanisms cause intraspecific competition to be stronger than interspecific competition. This simple principle has traditionally been applied to tests of local coexistence in a narrow range of ecological systems. However, new theory founded on the invasion criterion is emerging across ecological fields ranging from eco-evolutionary dynamics to global change to macroecology. Concurrently, straightforward methods for testing the invasion criterion have been proposed, but remain underused. Here, we identify the invasion criterion as a common thread linking emerging ecological theory, and we bring this theory together with the methods that can be used to test it.

Cryptic dispersal networks shape biodiversity in an invaded landscape.

Species interact with the physical world in complex ways, and life-history strategies could cause species to differ in how they experience the connectedness of the same landscape. As a consequence, dispersal limitation might be present but not captured by distance-based measures of connectivity. To test these ideas, we surveyed plant communities that live on discrete patches of serpentine habitat embedded within an invaded nonserpentine habitat matrix. Species in these communities differ in dispersal mode (gravity, animal, or wind); thus we used satellite imagery to quantify landscape features that might differentially influence connectivity for some dispersal- mode groups over others (surface streams, animal paths). Our data yielded two key insights: first, dispersal limitation appeared to be absent using a conventional distance-based measure of connectivity, but emerged after considering forms of landscape connectivity relevant to each dispersal mode. Second, the landscape variables that emerged as most important to each dispersal mode were generally consistent with our predictions based on species' putative dispersal vectors, but also included unexpected interactive effects. For example, the richness of animal-dispersed species was positively associated with animal connectivity when patches were close in space, but when patches were isolated, animals had a strong negative effect. This finding alludes to the reduced ability of animals to disperse seeds between suitable patches in invaded landscapes because of increased inter-patch distances. Real landscapes include complex spatial flows of energy and matter, which, as our work demonstrates, sets up ecological opportunity for organisms to differ in how they disperse in a common landscape.

Mechanisms for success after long-term nutrient enrichment in a boreal forest understory.

Global levels of reactive nitrogen are predicted to rise in the coming decades as a result of increased deposition from the burning of fossil fuels and the large-scale conversion of nitrogen into a useable form for agriculture. Many plant communities respond strongly to increases in soil nitrogen, particularly in northern ecosystems where nitrogen levels are naturally very low. An experiment in northern Canada that was initiated in 1990 has been investigating the effects of long-term nutrient enrichment (fertilizer added annually) on a boreal forest understory community. We used this experiment to investigate why some species increase in abundance under nutrient enrichment whereas others decline. We focused on four species that differed in their responses to fertilization: Mertensia paniculata and Epilobium angustifolium increased in abundance, Achillea millefolium remained relatively constant and Festuca altaica declined. We hypothesized that the two species that were successful in the new high-nutrient, light-limited environment would be taller, have higher specific leaf area, change phenology by growing earlier in the season and be more morphologically plastic than their less successful counterparts. We compared plant height, specific leaf area, growth spurt date and allocation to leaves in plants grown in control and fertilized plots. We demonstrated that each of the two species that came to dominate fertilized plots has a different combination of traits and responses that likely gave them a competitive advantage; M. paniculata has the highest specific leaf area of the four species whereas E. angustifolium is tallest and exhibits morphological plasticity when fertilized by increasing biomass allocation to leaves. These results indicate that rather than one strategy determining success when nutrients become available, a variety of traits and responses may contribute to a species' ability to persist in a nutrient-enriched boreal forest understory.