Occasional long distance dispersal increases spatial synchrony of population cycles.

Spatially separated populations of the same species often exhibit correlated fluctuations in abundance, a phenomenon known as spatial synchrony. Dispersal can generate spatial synchrony. In nature, most individuals disperse short distances with a minority dispersing long distances. The effect of occasional long distance dispersal on synchrony is untested, and theoretical predictions are contradictory. Occasional long distance dispersal might either increase both overall synchrony and the spatial scale of synchrony, or reduce them. We conducted a protist microcosm experiment to test whether occasional long distance dispersal increases or decreases overall synchrony and the spatial scale of synchrony. We assembled replicate 15-patch ring metapopulations of the protist predator Euplotes patella and its protist prey Tetrahymena pyriformis. All metapopulations experienced the same dispersal rate, but differed in dispersal distance. Some metapopulations experienced strictly short distance (nearest neighbour) dispersal, others experienced a mixture of short- and long distance dispersal. Occasional long distance dispersal increased overall spatial synchrony and the spatial scale of synchrony for both prey and predators, though the effects were not statistically significant for predators. As predicted by theory, dispersal generated spatial synchrony by entraining the phases of the predator-prey cycles in different patches, a phenomenon known as phase locking. Our results are consistent with theoretical models predicting that occasional long distance dispersal increases spatial synchrony. However, our results also illustrate that the spatial scale of synchrony need not match the spatial scale of the processes generating synchrony. Even strictly short distance dispersal maintained high spatial synchrony for many generations at spatial scales much longer than the dispersal distance, thanks to phase locking.

Effects of intraspecific phenotypic variation on species coexistence.

Intraspecific variation can promote or inhibit species coexistence, both by increasing species' competitive abilities, and by altering the relative strengths of intraspecific and interspecific competition. Effects of intraspecific variation on coexistence can occur via complementarity of different variants, and via a selection effect: initially-variable populations are more likely to contain highly competitive variants that might determine the ability of the population as a whole to both invade and resist invasion. We tested the effects of intraspecific variation and composition on coexistence by assaying the mutual invasibility of populations of two competing bean weevil species (Callosobruchus maculatus and C. chinensis) when each was initiated with one, three, or five genetically- and phenotypically-distinct lineages. Our results reveal that intraspecific variation is a double-edged sword for species coexistence. Increasing intraspecific variation increased species' abilities to invade, and to resist invasion, via selection effects and intraspecific niche complementarity among conspecific lineages, thereby creating the potential for exclusion among mismatched competitors. But intraspecific variation also increased the scope for resource partitioning, creating the potential for stable coexistence. Stable coexistence occurred only when intraspecific variation caused species to exhibit both relatively evenly-matched competitive abilities and sufficiently-strong resource partitioning. Our work explains the conflicting results of previous studies.

From Here to Eternity--The Theory and Practice of a Really Long Experiment.

In February 1988, Richard Lenski set up 12 replicate populations of a single genotype of Escherichia coli in a simple nutrient medium. He has been following their evolution ever since. Here, Lenski answers provocative questions from Jeremy Fox about his iconic "Long-Term Evolution Experiment" (LTEE). The LTEE is a remarkable case study of the interplay of determinism and chance in evolution-and in the conduct of science.

Moving forward in circles: challenges and opportunities in modelling population cycles.

Population cycling is a widespread phenomenon, observed across a multitude of taxa in both laboratory and natural conditions. Historically, the theory associated with population cycles was tightly linked to pairwise consumer-resource interactions and studied via deterministic models, but current empirical and theoretical research reveals a much richer basis for ecological cycles. Stochasticity and seasonality can modulate or create cyclic behaviour in non-intuitive ways, the high-dimensionality in ecological systems can profoundly influence cycling, and so can demographic structure and eco-evolutionary dynamics. An inclusive theory for population cycles, ranging from ecosystem-level to demographic modelling, grounded in observational or experimental data, is therefore necessary to better understand observed cyclical patterns. In turn, by gaining better insight into the drivers of population cycles, we can begin to understand the causes of cycle gain and loss, how biodiversity interacts with population cycling, and how to effectively manage wildly fluctuating populations, all of which are growing domains of ecological research.

Abundance of common species, not species richness, drives delivery of a real-world ecosystem service.

Biodiversity-ecosystem functioning experiments have established that species richness and composition are both important determinants of ecosystem function in an experimental context. Determining whether this result holds for real-world ecosystem services has remained elusive, however, largely due to the lack of analytical methods appropriate for large-scale, associational data. Here, we use a novel analytical approach, the Price equation, to partition the contribution to ecosystem services made by species richness, composition and abundance in four large-scale data sets on crop pollination by native bees. We found that abundance fluctuations of dominant species drove ecosystem service delivery, whereas richness changes were relatively unimportant because they primarily involved rare species that contributed little to function. Thus, the mechanism behind our results was the skewed species-abundance distribution. Our finding that a few common species, not species richness, drive ecosystem service delivery could have broad generality given the ubiquity of skewed species-abundance distributions in nature.

The extended Price equation quantifies species selection on mammalian body size across the Palaeocene/Eocene Thermal Maximum.

Species selection, covariation of species' traits with their net diversification rates, is an important component of macroevolution. Most studies have relied on indirect evidence for its operation and have not quantified its strength relative to other macroevolutionary forces. We use an extension of the Price equation to quantify the mechanisms of body size macroevolution in mammals from the latest Palaeocene and earliest Eocene of the Bighorn and Clarks Fork Basins of Wyoming. Dwarfing of mammalian taxa across the Palaeocene/Eocene Thermal Maximum (PETM), an intense, brief warming event that occurred at approximately 56 Ma, has been suggested to reflect anagenetic change and the immigration of small bodied-mammals, but might also be attributable to species selection. Using previously reconstructed ancestor-descendant relationships, we partitioned change in mean mammalian body size into three distinct mechanisms: species selection operating on resident mammals, anagenetic change within resident mammalian lineages and change due to immigrants. The remarkable decrease in mean body size across the warming event occurred through anagenetic change and immigration. Species selection also was strong across the PETM but, intriguingly, favoured larger-bodied species, implying some unknown mechanism(s) by which warming events affect macroevolution.

Phase-locking and environmental fluctuations generate synchrony in a predator-prey community.

Spatially synchronized fluctuations in system state are common in physical and biological systems ranging from individual atoms to species as diverse as viruses, insects and mammals. Although the causal factors are well known for many synchronized phenomena, several processes concurrently have an impact on spatial synchrony of species, making their separate effects and interactions difficult to quantify. Here we develop a general stochastic model of predator-prey spatial dynamics to predict the outcome of a laboratory microcosm experiment testing for interactions among all known synchronizing factors: (1) dispersal of individuals between populations; (2) spatially synchronous fluctuations in exogenous environmental factors (the Moran effect); and (3) interactions with other species (for example, predators) that are themselves spatially synchronized. The Moran effect synchronized populations of the ciliate protist Tetrahymena pyriformis; however, dispersal only synchronized prey populations in the presence of the predator Euplotes patella. Both model and data indicate that synchrony depends on cyclic dynamics generated by the predator. Dispersal, but not the Moran effect, 'phase-locks' cycles, which otherwise become 'decoherent' and drift out of phase. In the absence of cycles, phase-locking is not possible and the synchronizing effect of dispersal is negligible. Interspecific interactions determine population synchrony, not by providing an additional source of synchronized fluctuations, but by altering population dynamics and thereby enhancing the action of dispersal. Our results are robust to wide variation in model parameters representative of many natural predator-prey or host-pathogen systems. This explains why cyclic systems provide many of the most dramatic examples of spatial synchrony in nature.

Species richness and the temporal stability of biomass production: a new analysis of recent biodiversity experiments.

The relationship between biological diversity and ecological stability has fascinated ecologists for decades. Determining the generality of this relationship, and discovering the mechanisms that underlie it, are vitally important for ecosystem management. Here, we investigate how species richness affects the temporal stability of biomass production by reanalyzing 27 recent biodiversity experiments conducted with primary producers. We find that, in grasslands, increasing species richness stabilizes whole-community biomass but destabilizes the dynamics of constituent populations. Community biomass is stabilized because species richness impacts mean biomass more strongly than its variance. In algal communities, species richness has a minimal effect on community stability because richness affects the mean and variance of biomass nearly equally. Using a new measure of synchrony among species, we find that for both grasslands and algae, temporal correlations in species biomass are lower when species are grown together in polyculture than when grown alone in monoculture. These results suggest that interspecific interactions tend to stabilize community biomass in diverse communities. Contrary to prevailing theory, we found no evidence that species' responses to environmental variation in monoculture predicted the strength of diversity's stabilizing effect. Together, these results deepen our understanding of when and why increasing species richness stabilizes community biomass.

Synchronous dynamics of zooplankton competitors prevail in temperate lake ecosystems.

Although competing species are expected to exhibit compensatory dynamics (negative temporal covariation), empirical work has demonstrated that competitive communities often exhibit synchronous dynamics (positive temporal covariation). This has led to the suggestion that environmental forcing dominates species dynamics; however, synchronous and compensatory dynamics may appear at different length scales and/or at different times, making it challenging to identify their relative importance. We compiled 58 long-term datasets of zooplankton abundance in north-temperate and sub-tropical lakes and used wavelet analysis to quantify general patterns in the times and scales at which synchronous/compensatory dynamics dominated zooplankton communities in different regions and across the entire dataset. Synchronous dynamics were far more prevalent at all scales and times and were ubiquitous at the annual scale. Although we found compensatory dynamics in approximately 14% of all combinations of time period/scale/lake, there were no consistent scales or time periods during which compensatory dynamics were apparent across different regions. Our results suggest that the processes driving compensatory dynamics may be local in their extent, while those generating synchronous dynamics operate at much larger scales. This highlights an important gap in our understanding of the interaction between environmental and biotic forces that structure communities.

The dynamics of community assembly under sudden mixing in experimental microcosms.

Landscape connectivity has been shown to alter community assembly and its consequences. Here we examine how strong, sudden changes in connectivity may affect community assembly by conducting experiments on the effects of "community mixing," situations where previously isolated communities become completely connected with consequent community reorganization. Previous theory indicates that assembly history dictates the outcome of mixing: mixing randomly assembled communities leads to a final community with random representation from the original communities, while mixing communities that were assembled via a long history of colonizations and extinctions leads to strong asymmetry, with one community dominating the other. It also predicts that asymmetry should be stronger in the presence of predators in the system. We experimentally tested and explored this theory by mixing aquatic microcosms inhabited by a complex food web of heterotrophic protists, and algae. Our results confirm the prediction that long assembly history can produce asymmetry under mixing and suggest these dynamics could be important in natural systems. However, in contrast to previous theory we also found asymmetry weaker under mixing of communities with more complex trophic structure.

Biodiversity simultaneously enhances the production and stability of community biomass, but the effects are independent.

To predict the ecological consequences of biodiversity loss, researchers have spent much time and effort quantifying how biological variation affects the magnitude and stability of ecological processes that underlie the functioning of ecosystems. Here we add to this work by looking at how biodiversity jointly impacts two aspects of ecosystem functioning at once: (1) the production of biomass at any single point in time (biomass/area or biomass/ volume), and (2) the stability of biomass production through time (the CV of changes in total community biomass through time). While it is often assumed that biodiversity simultaneously enhances both of these aspects of ecosystem functioning, the joint distribution of data describing how species richness regulates productivity and stability has yet to be quantified. Furthermore, analyses have yet to examine how diversity effects on production covary with diversity effects on stability. To overcome these two gaps, we reanalyzed the data from 34 experiments that have manipulated the richness of terrestrial plants or aquatic algae and measured how this aspect of biodiversity affects community biomass at multiple time points. Our reanalysis confirms that biodiversity does indeed simultaneously enhance both the production and stability of biomass in experimental systems, and this is broadly true for terrestrial and aquatic primary producers. However, the strength of diversity effects on biomass production is independent of diversity effects on temporal stability. The independence of effect sizes leads to two important conclusions. First, while it may be generally true that biodiversity enhances both productivity and stability, it is also true that the highest levels of productivity in a diverse community are not associated with the highest levels of stability. Thus, on average, diversity does not maximize the various aspects of ecosystem functioning we might wish to achieve in conservation and management. Second, knowing how biodiversity affects productivity gives no information about how diversity affects stability (or vice versa). Therefore, to predict the ecological changes that occur in ecosystems after extinction, we will need to develop separate mechanistic models for each independent aspect of ecosystem functioning.

The existence and strength of higher order interactions is sensitive to environmental context.

One strategy for understanding the dynamics of any complex system, such as a community of competing species, is to study the dynamics of parts of the system in isolation. Ecological communities can be decomposed into single species, and pairs of interacting species. This reductionist strategy assumes that whole-community dynamics are predictable and explainable from knowledge of the dynamics of single species and pairs of species. This assumption will be violated if higher order interactions (HOIs) are strong. Theory predicts that HOIs should be common. But it is difficult to detect HOIs, and to infer their long-term consequences for species coexistence, solely from short-term data. I conducted a protist microcosm experiment to test for HOIs among competing bacterivorous ciliates, and test the sensitivity of HOIs to environmental context. I grew three competing ciliate species in all possible combinations at each of two resource enrichment levels, and used the population dynamic data from the one- and two-species treatments to parameterize a competition model at each enrichment level. I then compared the predictions of the parameterized model to the dynamics of the whole community (three-species treatment). I found that the existence, and thus strength, of HOIs was environment dependent. I found a strong HOI at low enrichment, which enabled the persistence of a species that would otherwise have been competitively excluded. At high enrichment, three-species dynamics could be predicted from a parameterized model of one- and two-species dynamics, provided that the model accounted for nonlinear intraspecific density dependence. The results provide one of the first rigorous demonstrations of the long-term consequences of HOIs for species coexistence, and demonstrate the context dependence of HOIs. HOIs create difficult challenges for predicting and explaining species coexistence in nature.

How much does the typical ecological meta-analysis overestimate the true mean effect size?

Many primary research studies in ecology are underpowered, providing very imprecise estimates of effect size. Meta-analyses partially mitigate this imprecision by combining data from different studies. But meta-analytic estimates of mean effect size may still remain imprecise, particularly if the meta-analysis includes a small number of studies. Imprecise, large-magnitude estimates of mean effect size from small meta-analyses likely would shrink if additional studies were conducted (regression towards the mean). Here, I propose a way to estimate and correct this regression to the mean, using meta-meta-analysis (meta-analysis of meta-analyses). Hierarchical random effects meta-meta-analysis shrinks estimated mean effect sizes from different meta-analyses towards the grand mean, bringing those estimated means closer on average to their unknown true values. The intuition is that, if a meta-analysis reports a mean effect size much larger in magnitude than that reported by other meta-analyses, that large mean effect size likely is an overestimate. This intuition holds even if different meta-analyses of different topics have different true mean effect sizes. Drawing on a compilation of data from hundreds of ecological meta-analyses, I find that the typical (median) ecological meta-analysis overestimates the absolute magnitude of the true mean effect size by ~10%. Some small ecological meta-analyses overestimate the magnitude of the true mean effect size by >50%. Meta-meta-analysis is a promising tool for improving the accuracy of meta-analytic estimates of mean effect size, particularly estimates based on just a few studies.

Decline effects are rare in ecology.

The scientific evidence base on any given topic changes over time as more studies are published. Currently, there is widespread concern about nonrandom, directional changes over time in the scientific evidence base associated with many topics. In particular, if studies finding large effects (e.g., large differences between treatment and control means) tend to get published quickly, while small effects tend to get published slowly, the net result will be a decrease over time in the estimated magnitude of the mean effect size, known as a "decline effect." If decline effects are common, then the published scientific literature will provide a biased and misleading guide to management decisions, and to the allocation of future research effort. We compiled data from 466 meta-analyses in ecology to look for evidence of decline effects. We found that decline effects are rare. Only ~5% of ecological meta-analyses truly exhibit a directional change in mean effect size over time arising for some reason other than random chance, usually but not always in the direction of decline. Most apparent directional changes in mean effect size over time are attributable to regression to the mean, consistent with primary studies being published in random order with respect to the effect sizes they report. Our results are good news: decline effects are the exception to the rule in ecology. Identifying and rectifying rare cases of true decline effects remains an important task, but ecologists should not overgeneralize from anecdotal reports of decline effects.

Phase locking, the Moran effect and distance decay of synchrony: experimental tests in a model system.

Spatially separated populations of many species fluctuate synchronously. Synchrony typically decays with increasing interpopulation distance. Spatial synchrony, and its distance decay, might reflect distance decay of environmental synchrony (the Moran effect), and/or short-distance dispersal. However, short-distance dispersal can synchronize entire metapopulations if within-patch dynamics are cyclic, a phenomenon known as phase locking. We manipulated the presence/absence of short-distance dispersal and spatially decaying environmental synchrony and examined their separate and interactive effects on the synchrony of the protist prey species Tetrahymena pyriformis growing in spatial arrays of patches (laboratory microcosms). The protist predator Euplotes patella consumed Tetrahymena and generated predator-prey cycles. Dispersal increased prey synchrony uniformly over both short and long distances, and did so by entraining the phases of the predator-prey cycles. The Moran effect also increased prey synchrony, but only over short distances where environmental synchrony was strongest, and did so by increasing the synchrony of stochastic fluctuations superimposed on the predator-prey cycle. Our results provide the first experimental demonstration of distance decay of synchrony due to distance decay of the Moran effect. Distance decay of the Moran effect likely explains distance decay of synchrony in many natural systems. Our results also provide an experimental demonstration of long-distance phase locking, and explain why cyclic populations provide many of the most dramatic examples of long-distance spatial synchrony in nature.

Adaptive dynamics of competition for nutritionally complementary resources: character convergence, displacement, and parallelism.

Consumers acquire essential nutrients by ingesting the tissues of resource species. When these tissues contain essential nutrients in a suboptimal ratio, consumers may benefit from ingesting a mixture of nutritionally complementary resource species. We investigate the joint ecological and evolutionary consequences of competition for complementary resources, using an adaptive dynamics model of two consumers and two resources that differ in their relative content of two essential nutrients. In the absence of competition, a nutritionally balanced diet rarely maximizes fitness because of the dynamic feedbacks between uptake rate and resource density, whereas in sympatry, nutritionally balanced diets maximize fitness because competing consumers with different nutritional requirements tend to equalize the relative abundances of the two resources. Adaptation from allopatric to sympatric fitness optima can generate character convergence, divergence, and parallel shifts, depending not on the degree of diet overlap but on the match between resource nutrient content and consumer nutrient requirements. Contrary to previous verbal arguments that suggest that character convergence leads to neutral stability, coadaptation of competing consumers always leads to stable coexistence. Furthermore, we show that incorporating costs of consuming or excreting excess nonlimiting nutrients selects for nutritionally balanced diets and so promotes character convergence. This article demonstrates that resource-use overlap has little bearing on coexistence when resources are nutritionally complementary, and it highlights the importance of using mathematical models to infer the stability of ecoevolutionary dynamics.

Coexistence mechanisms and the paradox of the plankton: quantifying selection from noisy data.

Many species of phytoplankton typically co-occur within a single lake, as do many zooplankton species (the "paradox of the plankton"). Long-term co-occurrence suggests stable coexistence. Coexistence requires that species be equally "fit" on average. Coexistence mechanisms can equalize species' long-term average fitnesses by reducing fitness differences to low levels at all times, and by causing species' relative fitness to fluctuate over time, thereby reducing differences in time-averaged fitness. We use recently developed time series analysis techniques drawn from population genetics to estimate the strength of net selection (time-averaged selection over a year) and fluctuating selection (an index of the variation in selection throughout the year) in natural plankton communities. Analysis of 99 annual time series of zooplankton species dynamics and 49 algal time series reveals that within-year net selection generally is statistically significant but ecologically weak. Rates of net selection are -10 times faster in laboratory competition experiments than in nature, indicating that natural coexistence mechanisms are strong. Most species experience significant fluctuating selection, indicating that fluctuation-dependent mechanisms may contribute to coexistence. Within-year net selection increases with enrichment, implying that among-year coexistence mechanisms such as trade-offs between competitive ability and resting egg production are especially important at high enrichment. Fluctuating selection also increases with enrichment but is independent of the temporal variance of key abiotic factors, suggesting that fluctuating selection does not emerge solely from variation in abiotic conditions, as hypothesized by Hutchinson. Nor does fluctuating selection vary among lake-years because more variable abiotic conditions comprise stronger perturbations to which species exhibit frequency-dependent responses, since models of this mechanism fail to reproduce observed patterns of fluctuating selection. Instead, fluctuating selection may arise from internally generated fluctuations in relative fitness, as predicted by models of fluctuation-dependent coexistence mechanisms. Our results place novel constraints on hypotheses proposed to explain the paradox of the plankton.

Experimental evolution of competing bean beetle species reveals long-term reversals of short-term evolution, but no consistent character displacement.

Interspecific competition for shared resources should select for evolutionary divergence in resource use between competing species, termed character displacement. Many purported examples of character displacement exist, but few completely rule out alternative explanations. We reared genetically diverse populations of two species of bean beetles, Callosobruchus maculatus and Callosobruchus chinensis, in allopatry and sympatry on a mixture of adzuki beans and lentils, and assayed oviposition preference and other phenotypic traits after four, eight, and twelve generations of (co)evolution. C. maculatus specializes on adzuki beans; the generalist C. chinensis uses both beans. C. chinensis growing in allopatry emerged equally from both bean species. In sympatry, the two species competing strongly and coexisted via strong realized resource partitioning, with C. chinensis emerging almost exclusively from lentils and C. maculatus emerging almost exclusively from adzuki beans. However, oviposition preferences, larval survival traits, and larval development rates in both beetle species did not vary consistently between allopatric versus sympatric treatments. Rather, traits evolved in treatment-independent fashion, with several traits exhibiting reversals in their evolutionary trajectories. For example, C. chinensis initially evolved a slower egg-to-adult development rate on adzuki beans in both allopatry and sympatry, then subsequently evolved back toward the faster ancestral development rate. Lack of character displacement is consistent with a previous similar experiment in bean beetles and may reflect lack of evolutionary trade-offs in resource use. However, evolutionary reversals were unexpected and remain unexplained. Together with other empirical and theoretical work, our results illustrate the stringency of the conditions for character displacement.

Character convergence under competition for nutritionally essential resources.

Resource competition is thought to drive divergence in resource use traits (character displacement) by generating selection favoring individuals able to use resources unavailable to others. However, this picture assumes nutritionally substitutable resources (e.g., different prey species). When species compete for nutritionally essential resources (e.g., different nutrients), theory predicts that selection drives character convergence. We used models of two species competing for two essential resources to address several issues not considered by existing theory. The models incorporated either slow evolutionary change in resource use traits or fast physiological or behavioral change. We report four major results. First, competition always generates character convergence, but differences in resource requirements prevent competitors from evolving identical resource use traits. Second, character convergence promotes coexistence. Competing species always attain resource use traits that allow coexistence, and adaptive trait change stabilizes the ecological equilibrium. In contrast, adaptation in allopatry never preadapts species to coexist in sympatry. Third, feedbacks between ecological dynamics and trait dynamics lead to surprising dynamical trajectories such as transient divergence in resource use traits followed by subsequent convergence. Fourth, under sufficiently slow trait change, ecological dynamics often drive one of the competitors to near extinction, which would prevent realization of long-term character convergence in practice.