Evolutionary origins for ecological patterns in space.

Historically, many biologists assumed that evolution and ecology acted independently because evolution occurred over distances too great to influence most ecological patterns. Today, evidence indicates that evolution can operate over a range of spatial scales, including fine spatial scales. Thus, evolutionary divergence across space might frequently interact with the mechanisms that also determine spatial ecological patterns. Here, we synthesize insights from 500 eco-evolutionary studies and develop a predictive framework that seeks to understand whether and when evolution amplifies, dampens, or creates ecological patterns. We demonstrate that local adaptation can alter everything from spatial variation in population abundances to ecosystem properties. We uncover 14 mechanisms that can mediate the outcome of evolution on spatial ecological patterns. Sometimes, evolution amplifies environmental variation, especially when selection enhances resource uptake or patch selection. The local evolution of foundation or keystone species can create ecological patterns where none existed originally. However, most often, we find that evolution dampens existing environmental gradients, because local adaptation evens out fitness across environments and thus counteracts the variation in associated ecological patterns. Consequently, evolution generally smooths out the underlying heterogeneity in nature, making the world appear less ragged than it would be in the absence of evolution. We end by highlighting the future research needed to inform a fully integrated and predictive biology that accounts for eco-evolutionary interactions in both space and time.

Regional neutrality evolves through local adaptive niche evolution.

Biodiversity in natural systems can be maintained either because niche differentiation among competitors facilitates stable coexistence or because equal fitness among neutral species allows for their long-term cooccurrence despite a slow drift toward extinction. Whereas the relative importance of these two ecological mechanisms has been well-studied in the absence of evolution, the role of local adaptive evolution in maintaining biological diversity through these processes is less clear. Here we study the contribution of local adaptive evolution to coexistence in a landscape of interconnected patches subject to disturbance. Under these conditions, early colonists to empty patches may adapt to local conditions sufficiently fast to prevent successful colonization by other preadapted species. Over the long term, the iteration of these local-scale priority effects results in niche convergence of species at the regional scale even though species tend to monopolize local patches. Thus, the dynamics evolve from stable coexistence through niche differentiation to neutral cooccurrence at the landscape level while still maintaining strong local niche segregation. Our results show that neutrality can emerge at the regional scale from local, niche-based adaptive evolution, potentially resolving why ecologists often observe neutral distribution patterns at the landscape level despite strong niche divergence among local communities.

Temporal stability vs. community matrix measures of stability and the role of weak interactions.

Relationships between different measures of stability are not well understood in part because empiricists and theoreticians tend to measure different aspects and most studies only explore a single form of stability. Using time-series data from experimental plankton communities, we compared temporal stability typically measured by empiricists (coefficient of variation in biomass) to stability measures typically measured by theoreticians derived from the community matrix (asymptotic resilience, initial resilience and intrinsic stochastic invariability) using first-order multivariate autoregressive models (MAR). Community matrices were also used to derive estimates of interaction strengths between plankton groups. We found no relationship between temporal stability and stability measures derived from the community matrix. Weaker interaction strengths were generally associated with higher stability for community matrix measures of stability, but were not consistently associated with higher temporal stability. Temporal stability and stability measures derived from the community matrix stability appear to represent different aspects of stability reflecting the multi-dimensionality of stability.

Dormancy in Metacommunities.

Although metacommunity ecology has improved our understanding of how dispersal affects community structure and dynamics across spatial scales, it has yet to adequately account for dormancy. Dormancy is a reversible state of reduced metabolic activity that enables temporal dispersal within the metacommunity. Dormancy is also a metacommunity-level process because it can covary with spatial dispersal and affect diversity across spatial scales. We develop a framework to integrate dispersal and dormancy, focusing on the covariation they exhibit, to predict how dormancy modifies the importance of species interactions, dispersal, and historical contingencies in metacommunities. We used empirical and modeling approaches to demonstrate the utility of this framework. We examined case studies of microcrustaceans in ephemeral ponds, where dormancy underlies metacommunity dynamics, and identified constraints on the dispersal and dormancy strategies of bromeliad-dwelling invertebrates. Using simulations, we showed that dormancy can alter classic metacommunity patterns of diversity in ways that depend on dispersal-dormancy covariation and spatiotemporal environmental variability. We propose that dormancy may also facilitate evolution-mediated priority effects if locally adapted seed banks prevent colonization by more dispersal-limited species. Last, we present testable predictions for the implications of dormancy in metacommunities, some of which may fundamentally alter our understanding of metacommunity ecology.

Integrating community assembly and biodiversity to better understand ecosystem function: the Community Assembly and the Functioning of Ecosystems (CAFE) approach.

The research of a generation of ecologists was catalysed by the recognition that the number and identity of species in communities influences the functioning of ecosystems. The relationship between biodiversity and ecosystem functioning (BEF) is most often examined by controlling species richness and randomising community composition. In natural systems, biodiversity changes are often part of a bigger community assembly dynamic. Therefore, focusing on community assembly and the functioning of ecosystems (CAFE), by integrating both species richness and composition through species gains, losses and changes in abundance, will better reveal how community changes affect ecosystem function. We synthesise the BEF and CAFE perspectives using an ecological application of the Price equation, which partitions the contributions of richness and composition to function. Using empirical examples, we show how the CAFE approach reveals important contributions of composition to function. These examples show how changes in species richness and composition driven by environmental perturbations can work in concert or antagonistically to influence ecosystem function. Considering how communities change in an integrative fashion, rather than focusing on one axis of community structure at a time, will improve our ability to anticipate and predict changes in ecosystem function.

Testing the keystone community concept: effects of landscape, patch removal, and environment on metacommunity structure.

Although the influence of regional processes on local patches is well studied, the influence of local patches and their spatial arrangement on regional processes is likely to be complex. One interesting idea is the keystone community concept (KCC); this posits that there may be some patches that have a disproportionately large effect on the metacommunity compared to other patches. We experimentally test the KCC by using replicate protist microcosm metacommunities with single-patch removals. Removing single patches had no effect on average community richness, evenness and biomass of our metacommunities, but did cause metacommunities to be assembled significantly less by local environmental conditions and more by spatial effects related to stochastic factors. Overall our results show that local patch removal can have large regional effects on structural processes, but indicate that more experiments are needed to find evidence of keystone communities.

Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystems attributes.

Recent work linking community structure and ecosystem function has primarily focused on the effects of local species richness but has neglected the dispersal-dependent processes of community assembly that are ultimately involved in determining community structure and its relation to ecosystems. Here we combine simple consumer-resource competition models and metacommunity theory with discussion of case studies to outline how spatial processes within metacommunities can alter community assembly and modify expectations about how species diversity and composition influence ecosystem attributes at local scales. We argue that when community assembly is strongly limited by dispersal, this can constrain ecosystem functioning by reducing positive selection effects (reducing the probability of the most productive species becoming dominant) even though it may often also enhance complementarity (favoring combinations of species that enhance production even though they may not individually be most productive). Conversely, excess dispersal with strong source-sink relations among heterogeneous habitats can reduce ecosystem functioning by swamping local filters that would normally favor better-suited species. Ecosystem function is thus most likely maximized at intermediate levels of dispersal where both of these effects are minimized. In this scenario, we find that the selection effect is maximized, while complementarity is often reduced and local diversity may often be relatively low. Our synthesis emphasizes that it is the entire set of community assembly processes that affect the functioning of ecosystems, not just the part that determines local species richness.

Herbivory enhances the diversity of primary producers in pond ecosystems.

Diversity of primary producer is often surprisingly high, despite few limiting factors such as nutrients and light to facilitate species coexistence. In theory, the presence of herbivores could increase the diversity of primary producers, resolving this "paradox of the plankton." Little experimental evidence supports this natural enemies hypothesis, but previous tests suffer from several deficiencies. Previous experiments often did not allow for multigeneration effects; utilized low diversity assemblages of herbivores; and limited opportunities for new primary producer and herbivore species to colonize and undergo species sorting that favors some species over others. Using pond plankton, we designed a mesocosm experiment that overcame these problems by allowing more time for interactions over multiple generations, openness to allow new colonists, and manipulated higher diversity of primary producers and grazers than have previous studies. With this design, the presence of zooplankton grazers doubled phytoplankton richness. The additional phytoplankton species in grazed mesocosms were larger, and therefore likely more grazer resistant. Furthermore, phytoplankton richness in grazed mesocosms was similar to that observed in natural ponds whereas it was much lower in mesocosms without grazers. However, stoichiometric imbalance caused by variation in nitrogen : phosphorus ratios and light supply did not alter phytoplankton richness. Therefore, grazers enhanced primary producer richness more strongly than ratios of nutrient supply (even though both grazing and ratios of resource supply altered composition of primary producer assemblages). Taken together, these experimental and field data show that grazing from a diverse assemblage of herbivores greatly elevated richness of phytoplankton producers in pond ecosystems.

Predators regulate prey species sorting and spatial distribution in microbial landscapes.

The role of predation in determining the metacommunity assembly model of prey communities is understudied relative to that of interspecific competition among prey. Previous work on metacommunity dynamics of competing species has shown that sorting by habitat patch type and spatial patterning can be affected by disturbances. Microcosms offer a useful model system to test the effect of multi-trophic interactions and disturbance on metacommunity dynamics. Here, we investigated the potential role of predators in enhancing or disrupting sorting and spatial pattern among prey in experimental landscapes. We exposed multi-trophic protist microcosm landscapes with one predator, two competing prey, two patch resource types, and localized dispersal to three disturbance regimes (none, low, and high). Then, we used variation partitioning and spatial clustering analysis to analyse the results. In contrast with previous experiments that did not manipulate predators, we found that patch type did not structure prey communities very well. Instead, we found that it was the distribution of the predator that most strongly predicted the composition of the prey community. The predator impacted species sorting by (1) preferentially consuming one prey, thereby acting as a strong local environmental driver, and by (2) indirectly magnifying the impact of patch food resources on the less preferred prey. The predator also enhanced spatial signal in the prey community because of its limited dispersal. Our results indicate that predators can strongly influence prey species sorting and spatial patterning in metacommunities in ways that would otherwise be attributed to stochastic effects, such as dispersal limitation or demographic drift. Therefore, whenever possible, predators should be explicitly included as separate explanatory factors in variation partitioning analyses.

Compensatory dynamics stabilize aggregate community properties in response to multiple types of perturbations.

Compensatory dynamics are an important suite of mechanisms that can stabilize community and ecosystem attributes in systems subject to environmental fluctuations. However, few experimental investigations of compensatory dynamics have addressed these mechanisms in systems of real-world complexity, and existing evidence relies heavily on correlative analyses, retrospective examination, and experiments in simple systems. We investigated the potential for compensatory dynamics to stabilize plankton communities in plankton mesocosm systems of real-world complexity. We employed four types of perturbations including two types of nutrient pulses, shading, and acidification. To quantify how communities responded to these perturbations, we used a measure of community-wide synchrony combined with spectral analysis that allowed us to assess timescale-specific community dynamics, for example, whether dynamics were synchronous at some timescales but compensatory at others. The 150-d experiment produced 32-point time series of all zooplankton taxa in the mesocosms. We then used those time series to evaluate total zooplankton biomass as an aggregate property and to evaluate community dynamics. For three of our four perturbation types, total zooplankton biomass was significantly less variable in systems with environmental variation than in constant environments. For the same three perturbation types, community-wide synchrony was much lower in fluctuating environments than in the constant environment, particularly at longer timescales (periods ≈ 60 d). Additionally, there were strong negative correlations between population temporal variances and the level of community-wide synchrony. Taken together, these results strongly imply that compensatory interactions between species stabilized total biomass in response to perturbations. Diversity did not differ significantly across either treatments or perturbation types, thus ruling out several classes of mechanisms driven by changes in diversity. We also used several pieces of secondary evidence to evaluate the particular mechanism behind compensatory responses since a wide variety of mechanisms are hypothesized to produce compensatory dynamics. We concluded that fluctuation dependent endogenous cycles that occur as a consequence of consumer-resource interactions in competitive communities were the most likely explanation for the compensatory dynamics observed in our experiment. As with our previous work, scale-dependent dynamics were also a key to understanding compensatory dynamics in these experimental communities.

Extensive cross-environment fitness variation lies along few axes of genetic variation in the model alga, Chlamydomonas reinhardtii.

Variation is essential to ecological and evolutionary dynamics, but genetic variation of quantitative traits may be concentrated in a limited number of dimensions, constraining ecoevolutionary dynamics. We describe high-dimension variation in natural accessions of the model alga, Chlamydomonas reinhardtii, and test the hypothesis that extensive fitness variation across 30 environments is constrained to a small number of axes. We used high-throughput phenotyping to investigate morphological, fitness, and genotype × environment (G × E) variation in 18 natural C. reinhardtii accessions in 30 environments. The organismal phenotypes of cell cycle, cell size, and phototactic behavior exhibited substantial genetic variation between lines, and we found up to 74-fold fitness variation across accessions and environments. Approximately 47% of the extensive G × E variation is accounted for by the first two principal components (PCs) of the G-matrix corresponding to covariation in metals response, nitrogen availability, or salt and nutrient response. The natural variation of C. reinhardtii accessions supports the hypothesis that, despite abundant genetic variation across single environments, the species' adaptive response should be constrained along few major axes of selection. These results highlight the utility of natural accessions for integrating ecoevolutionary and genetic research.

Species sorting and patch dynamics in harlequin metacommunities affect the relative importance of environment and space.

Metacommunity theory indicates that variation in local community structure can be partitioned into components including those related to local environmental conditions vs. spatial effects and that these can be quantified using statistical methods based on variation partitioning. It has been hypothesized that joint associations of community composition with environment and space could be due to patch dynamics involving colonization-extinction processes in environmentally heterogeneous landscapes but this has yet to be theoretically shown. We develop a two-patch, type-two, species competition model in such a "harlequin" landscape (where different patches have different environments) to evaluate how composition is related to environmental and spatial effects as a function of background extinction rate. Using spatially implicit analytical models, we find that the environmental association of community composition declines with extinction rate as expected. Using spatially explicit simulation models, we further find that there is an increase in the spatial structure with extinction due to spatial patterning into clusters that are not related to environmental conditions but that this increase is limited. Natural metacommunities often show both environment and spatial determination even under conditions of relatively high isolation and these could be more easily explained by our model than alternative metacommunity models.

Disturbance-mediated colonization-extinction dynamics in experimental protist metacommunities.

Colonization-extinction dynamics and species sorting among habitats deter- mine the distribution of species within metacommunities. Theory suggests that disturbances reduce the importance of species sorting and enhance spatial patterning and stochastic effects, however this has not yet been experimentally shown. We examined how extinctions in a heterogeneous landscape of patches affects the influence of environmental, spatial, and stochastic factors on community composition in a simple two-species, two-habitat, protist metacommunity where each species dominates in a different habitat type. We imposed four different levels of random extinctions on local patches and monitored changes in the metacommunity through time. We found that near-steady state patterns of community variability developed relatively rapidly (within nine colonization-extinction cycles) and that increased extinction rate produced altered patterns of community regulation by reducing environmental control and increasing spatial and stochastic effects. Our results indicate a possible explanation for the combination of environmental, spatial and stochastic effects observed in natural metacommunities.

Effects of local negative feedbacks on the evolution of species within metacommunities.

Local negative feedbacks occur when the occupation of a site by a species decreases the subsequent fitness of related individuals compared to potential competitors. Such negative feedbacks can enhance diversity by changing the spatial structure of the environment. The conditions, however, involve dispersive, environmental and evolutionary processes in complex interactive ways. We introduce a model that accounts for four mechanisms: colonisation-competition-extinction ecological dynamics, evolutionary dynamics, local negative feedbacks and environmental averaging. Three qualitatively distinct dynamics are possible, one dominated by specialists, another dominated by generalists and an intermediate situation exhibiting taxon cycles. We discuss how metacommunity diversity, macro-ecological patterns and environmental patterning are linked to the three qualitative dynamics. The model provides classical shapes for morph-abundance distributions, or diversity-area relationships. Diversity can be high when specialists dominate or when taxon cycles happen. Finally, local negative feedbacks often yield fine-grain environments for taxon cycle dynamics and coarse-grain environments when generalists dominate.

Multiple diversity-stability mechanisms enhance population and community stability in aquatic food webs.

Biodiversity has been shown to increase the temporal stability of community and ecosystem attributes through multiple mechanisms, but these same mechanisms make less consistent predictions about the effects of richness on population stability. The overall effects of biodiversity on population and community stability will therefore depend on the dominant mechanisms that are likely to vary with the nature of biodiversity loss and the degree of environmental variability. We conducted a mesocosm experiment in which we generated a gradient in zooplankton species richness by directly manipulating dominant species and by allowing/preventing immigration from a metacommunity. The mesocosms were maintained under either constant or variable nutrient environments. Population, community, and ecosystem data were collected for five months. We found that zooplankton population and community stability is enhanced in species-rich communities in both constant and variable environments. Species richness increased primarily through the addition of species with low abundance. The communities that were connected to a metacommunity via immigration were the most diverse and the most stable, indicating the importance of both metacommunity dynamics and rare species for stability. We found little evidence for selection effects or overyielding as stabilizing forces. We did find support for asynchronous dynamics and statistical averaging, both of which predict destabilizing effects at the population level. We also found support for weak interactions, which predicts that both populations and communities will become more stable as richness increases. In order to understand the effects of biodiversity loss on stability, we will need to understand when different stabilizing mechanisms tend to operate but also how multiple mechanisms interact.

Novel community data in ecology-properties and prospects.

New technologies for monitoring biodiversity such as environmental (e)DNA, passive acoustic monitoring, and optical sensors promise to generate automated spatiotemporal community observations at unprecedented scales and resolutions. Here, we introduce 'novel community data' as an umbrella term for these data. We review the emerging field around novel community data, focusing on new ecological questions that could be addressed; the analytical tools available or needed to make best use of these data; and the potential implications of these developments for policy and conservation. We conclude that novel community data offer many opportunities to advance our understanding of fundamental ecological processes, including community assembly, biotic interactions, micro- and macroevolution, and overall ecosystem functioning.

Predation inhibits the positive effect of dispersal on intraspecific and interspecific synchrony in pond metacommunities.

Recent interest in the ecological drivers of compensatory and synchronous population dynamics has provided an improved yet incomplete understanding of local and regional population oscillations in response to variable environments. Here, we evaluate the effect of dispersal rate and spatiotemporal heterogeneity in predation by the selective planktivore, bluegill sunfish (Lepomis macrochirus), on local and regional dynamics of zooplankton in pond metacommunities. A metacommunity consisted of three pond mesocosm communities, one with constant presence of predators, one without predators, and one with alternating presence-absence of predators. The three communities were connected at either no, low (0.7% per day), or high (20% per day) planktonic dispersal. Results demonstrate that heterogeneous predation (1) prevents spatial synchrony among prey populations across local communities, (2) disrupts the synchronous population dynamics within communities produced by dispersal, and (3) induces local compensatory dynamics between species within communities regardless of dispersal rate. Taken together, the results emphasize that spatiotemporal heterogeneity in selective predation can inhibit both intraspecific and interspecific synchrony in metacommunities.

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.

Beyond the fish-Daphnia paradigm: testing the potential for pygmy backswimmers (Neoplea striola) to cause trophic cascades in subtropical ponds.

Trophic cascades, or indirect effects of predators on non-adjacent lower trophic levels, are a classic phenomenon in ecology, and are thought to be strongest in aquatic ecosystems. Most research on freshwater trophic cascades focused on temperate lakes, where fish are present and where Daphnia frequently dominate the zooplankton community. These studies identified that Daphnia often play a key role in facilitating trophic cascades by linking fish to algae with strong food web interactions. However, Daphnia are rare or absent in most tropical and subtropical lowland freshwaters, and fish are absent from small and temporary water bodies, where invertebrates fill the role of top predator. While invertebrate predators are ubiquitous in freshwater systems, most have received little attention in food web research. Therefore, we aimed to test whether trophic cascades are possible in small warmwater ponds where Daphnia are absent and small invertebrates are the top predators. We collected naturally occurring plankton communities from small fishless water bodies in central Texas and propagated them in replicate pond mesocosms. We removed zooplankton from some mesocosms, left the plankton community intact in others, and added one of two densities of the predaceous insect Neoplea striola to others. Following an incubation period, we then compared biomasses of plankton groups to assess food web effects between the trophic levels, including whether Neoplea caused a trophic cascade by reducing zooplankton. The zooplankton community became dominated by copepods which prefer large phytoplankton and exhibit a fast escape response. Perhaps due to these qualities of the copepods and perhaps due to other reasons such as high turbidity impairing predation, no evidence for food web effects were found other than somewhat weak evidence for zooplankton reducing large phytoplankton. More research is needed to understand the behavior and ecology of Neoplea, but trophic cascades may generally be weak or absent in fishless low latitude lowland water bodies where Daphnia are rare.

Linking community and ecosystem dynamics through spatial ecology.

Classical approaches to food webs focus on patterns and processes occurring at the community level rather than at the broader ecosystem scale, and often ignore spatial aspects of the dynamics. However, recent research suggests that spatial processes influence both food web and ecosystem dynamics, and has led to the idea of 'metaecosystems'. However, these processes have been tackled separately by 'food web metacommunity' ecology, which focuses on the movement of traits, and 'landscape ecosystem' ecology, which focuses on the movement of materials among ecosystems. Here, we argue that this conceptual gap must be bridged to fully understand ecosystem dynamics because many natural cases demonstrate the existence of interactions between the movements of traits and materials. This unification of concepts can be achieved under the metaecosystem framework, and we present two models that highlight how this framework yields novel insights. We then discuss patches, limiting factors and spatial explicitness as key issues to advance metaecosystem theory. We point out future avenues for research on metaecosystem theory and their potential for application to biological conservation.