The Evolution of Competitive Ability.

AbstractCompetition drives evolutionary change across taxa, but our understanding of how competitive differences among species directs the evolution of interspecific interactions remains incomplete. Verbal models assume that interspecific competition will select for reducing a species' sensitivity to competition with their opponent; however, they do not consider the potential for other demographic components of competitive ability to evolve, specifically, interspecific effects, intraspecific interactions, and intrinsic growth rates. To better understand how competitive ability evolves, we set out to explore how each component has evolved and whether their evolution has been constrained by trade-offs. By setting sympatric and allopatric populations of an annual grass in competition with a dominant invader, we demonstrate (1) that in response to interspecific competition, populations can evolve increased competitive ability through either reduced interspecific or, surprisingly, reduced intraspecific competition; (2) that trade-offs do not always constrain the evolution of competitive ability but rather that parameters may correlate in ways that mutually beget higher competitive ability; and (3) that the evolution of one species can influence the competitive ability of its opponent, a consequence of how competitive ability is defined ecologically. Overall, our results reveal the complexity with which demographic components evolve in response to interspecific competition and the impact past evolution can have on present-day interactions.

An Empiricist's Guide to Using Ecological Theory.

AbstractA scientific understanding of the biological world arises when ideas about how nature works are formalized, tested, refined, and then tested again. Although the benefits of feedback between theoretical and empirical research are widely acknowledged by ecologists, this link is still not as strong as it could be in ecological research. This is in part because theory, particularly when expressed mathematically, can feel inaccessible to empiricists who may have little formal training in advanced math. To address this persistent barrier, we provide a general and accessible guide that covers the basic, step-by-step process of how to approach, understand, and use ecological theory in empirical work. We first give an overview of how and why mathematical theory is created, then outline four specific ways to use both mathematical and verbal theory to motivate empirical work, and finally present a practical tool kit for reading and understanding the mathematical aspects of ecological theory. We hope that empowering empiricists to embrace theory in their work will help move the field closer to a full integration of theoretical and empirical research.

Scaling-up biodiversity-ecosystem functioning research.

A rich body of knowledge links biodiversity to ecosystem functioning (BEF), but it is primarily focused on small scales. We review the current theory and identify six expectations for scale dependence in the BEF relationship: (1) a nonlinear change in the slope of the BEF relationship with spatial scale; (2) a scale-dependent relationship between ecosystem stability and spatial extent; (3) coexistence within and among sites will result in a positive BEF relationship at larger scales; (4) temporal autocorrelation in environmental variability affects species turnover and thus the change in BEF slope with scale; (5) connectivity in metacommunities generates nonlinear BEF and stability relationships by affecting population  synchrony at local and regional scales; (6) spatial scaling in food web structure and diversity will generate scale dependence in ecosystem functioning. We suggest directions for synthesis that combine approaches in metaecosystem and metacommunity ecology and integrate cross-scale feedbacks. Tests of this theory may combine remote sensing with a generation of networked experiments that assess effects at multiple scales. We also show how anthropogenic land cover change may alter the scaling of the BEF relationship. New research on the role of scale in BEF will guide policy linking the goals of managing biodiversity and ecosystems.

Species Differences in Phenology Shape Coexistence.

Ecological theory produces opposing predictions about whether differences in the timing of life-history transitions, or "phenology," promote or limit coexistence. Phenological separation is predicted to create temporal niche differences, increasing coexistence, yet phenological separation could also competitively favor one species, increasing fitness differences and hindering coexistence. We experimentally manipulated relative germination timing, a critical phenological event, of two annual grass species, Vulpia microstachys and V. octoflora, to test these contrasting predictions. We parameterized a competition model to estimate within-season niche differences, fitness differences, and coexistence and to estimate coexistence when year-to-year fluctuations of germination timing occur. Increasing germination separation caused parallel changes in niche and fitness differences, with the net effect of weakening within-year coexistence. Both species experienced a competitive advantage by germinating earlier, and a 4-day head start allowed the generally inferior competitor to exclude the otherwise superior competitor. The overall consequence of germination separation was to limit coexistence within a given year, although year-to-year variation in the relative timing of germination was sufficient to support long-term coexistence. Our results clarify how phenological differences structure competitive interactions and highlight the need to quantify year-to-year variation in these differences to better understand species coexistence.

Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes.

Adaptation to local conditions can increase species' geographic distributions and rates of diversification, but which components of the environment commonly drive local adaptation-particularly the importance of biotic interactions-is unclear. Biotic interactions should drive local adaptation when they impose consistent divergent selection; if this is common, we expect transplant experiments to detect more frequent and stronger local adaptation when biotic interactions are left intact. We tested this hypothesis using a meta-analysis of transplant experiments from >125 studies (mostly of plants). Overall, local adaptation was common, and biotic interactions affected fitness. Nevertheless, local adaptation was neither more common nor stronger when biotic interactions were left intact, either between experimental treatments within studies (control vs. biotic interactions experimentally manipulated) or between studies that used natural versus biotically altered transplant environments. However, the effect of ameliorating negative interactions varied with latitude, suggesting that interactions may promote local adaptation more often in tropical than in temperate ecosystems, although few tropical studies were available to test this. Our results suggest that biotic interactions often fail to drive local adaptation even though they strongly affect fitness, perhaps because temperate biotic environments are unpredictable at the spatiotemporal scales required for local adaptation.

Experimental dispersal reveals characteristic scales of biodiversity in a natural landscape.

Ecological theory posits that dispersal among habitat patches links local communities and is a key "regional" process that maintains biological diversity. However, manipulations required to experimentally test regional processes are infeasible for most systems, and thus more work is needed to detect the scales at which regional processes manifest and their overall effect on diversity. In a Californian grassland, a hotspot for global biodiversity, we used a seed vacuum to increase dispersal at spatial scales varying from 1 m to 10 km while maintaining a realistic spatial structure of species pools and environmental conditions. We found that dispersal limitation has a profound influence on diversity; species richness increased with the spatial scale of seed mixing, doubling in plots that received seed from large (≥5 km) compared with small (≤5 m) scales. This increase in diversity corresponded to an increase in how well species distributions were explained by environmental conditions, from modest at small scales (R2 = 0.34) to strong at large scales (R2 = 0.52). Responses to the spatial scale of seed mixing were nonlinear, with no differences below 5 m or above 5 km. Nonlinearities were explained by homogeneity of environmental conditions below 5 m and by a lack of additional variation in the species pool above 5 km. Our approach of manipulating natural communities at different spatial scales reveals (i) nonlinear transitions in the importance of environmental sorting and dispersal, and (ii) the negative effects of dispersal limitation on local diversity, consistent with previous research suggesting that large numbers of species are headed toward regional extinction.

Towards a multi-trophic extension of metacommunity ecology.

Metacommunity theory provides an understanding of how spatial processes determine the structure and function of communities at local and regional scales. Although metacommunity theory has considered trophic dynamics in the past, it has been performed idiosyncratically with a wide selection of possible dynamics. Trophic metacommunity theory needs a synthesis of a few influential axis to simplify future predictions and tests. We propose an extension of metacommunity ecology that addresses these shortcomings by incorporating variability among trophic levels in 'spatial use properties'. We define 'spatial use properties' as a set of traits (dispersal, migration, foraging and spatial information processing) that set the spatial and temporal scales of organismal movement, and thus scales of interspecific interactions. Progress towards a synthetic predictive framework can be made by (1) documenting patterns of spatial use properties in natural food webs and (2) using theory and experiments to test how trophic structure in spatial use properties affects metacommunity dynamics.

The 'filtering' metaphor revisited: competition and environment jointly structure invasibility and coexistence.

'Filtering', or the reduction in species diversity that occurs because not all species can persist in all locations, is thought to unfold hierarchically, controlled by the environment at large scales and competition at small scales. However, the ecological effects of competition and the environment are not independent, and observational approaches preclude investigation into their interplay. We use a demographic approach with 30 plant species to experimentally test: (i) the effect of competition on species persistence in two soil moisture environments, and (ii) the effect of environmental conditions on mechanisms underlying competitive coexistence. We find that competitors cause differential species persistence across environments even when effects are lacking in the absence of competition, and that the traits which determine persistence depend on the competitive environment. If our study had been observational and trait-based, we would have erroneously concluded that the environment filters species with low biomass, shallow roots and small seeds. Changing environmental conditions generated idiosyncratic effects on coexistence outcomes, increasing competitive exclusion of some species while promoting coexistence of others. Our results highlight the importance of considering environmental filtering in the light of, rather than in isolation from, competition, and challenge community assembly models and approaches to projecting future species distributions.

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.

Species coexistence: macroevolutionary relationships and the contingency of historical interactions.

Evolutionary biologists since Darwin have hypothesized that closely related species compete more intensely and are therefore less likely to coexist. However, recent theory posits that species diverge in two ways: either through the evolution of 'stabilizing differences' that promote coexistence by causing individuals to compete more strongly with conspecifics than individuals of other species, or through the evolution of 'fitness differences' that cause species to differ in competitive ability and lead to exclusion of the weaker competitor. We tested macroevolutionary patterns of divergence by competing pairs of annual plant species that differ in their phylogenetic relationships, and in whether they have historically occurred in the same region or different regions (sympatric versus allopatric occurrence). For sympatrically occurring species pairs, stabilizing differences rapidly increased with phylogenetic distance. However, fitness differences also increased with phylogenetic distance, resulting in coexistence outcomes that were unpredictable based on phylogenetic relationships. For allopatric species, stabilizing differences showed no trend with phylogenetic distance, whereas fitness differences increased, causing coexistence to become less likely among distant relatives. Our results illustrate the role of species' historical interactions in shaping how phylogenetic relationships structure competitive dynamics, and offer an explanation for the evolution of invasion potential of non-native species.

Hidden responses to environmental variation: maternal effects reveal species niche dimensions.

Species responses to fluctuating environments structure population and community dynamics in variable ecosystems. Although offspring number is commonly used to measure these responses, maternal effects on offspring quality may be an important but largely unrecognised determinant of long-term population growth. We selected 29 species across a Mediterranean annual plant phylogeny, and grew populations of each species in wet and dry conditions to determine responses in seed number and maternal effects (seed size, seed dormancy, and seedling growth). Maternal effects were evident in over 40% of species, but only 24% responded through seed number. Despite a strong trade-off between seed size and seed number among species, there was no consistent trade-off within species; we observed correlations that ranged from positive to negative. Overall, species in this plant guild show a complex range of responses to environmental variation that may be underestimated when only seed number responses are considered.

Landscape use by large grazers in a grassland is restructured by wildfire.

Animals navigate landscapes based on perceived risks vs. rewards, as inferred from features of the landscape. In the wild, knowing how strongly animal movement is directed by landscape features is difficult to ascertain but widespread disturbances such as wildfires can serve as natural experiments. We tested the hypothesis that wildfires homogenize the risk/reward landscape, causing movement to become less directed, given that fires reduce landscape complexity as habitat structures (e.g., tree cover, dense brush) are burned. We used satellite imagery of a research reserve in Northern California to count and categorize paths made primarily by mule deer (Odocoileus hemionus) in grasslands. Specifically, we compared pre-wildfire (August 2014) and post-wildfire (September 2018) image history layers among locations that were or were not impacted by wildfire (i.e., a Before/After Control/Impact design). Wildfire significantly altered spatial patterns of deer movement: more new paths were gained and more old paths were lost in areas of the reserve that were impacted by wildfire; movement patterns became less directed in response to fire, suggesting that the risk/reward landscape became more homogenous, as hypothesized. We found evidence to suggest that wildfire affects deer populations at spatial scales beyond their scale of direct impact and raises the interesting possibility that deer perceive risks and rewards at different spatial scales. In conclusion, our study provides an example of how animals integrate spatial information from the environment to make movement decisions, setting the stage for future work on the broader ecological implications for populations, communities, and ecosystems, an emerging interest in ecology.

Niche Theory as an Underutilized Resource for the Study of Adaptive Radiations.

Biologists are often stuck between two opposing questions: Why are there so many species and why are there not more? Although these questions apply to the maintenance of existing species, they equally apply to the formation of new ones. The more species specialize in terms of their niches, the more opportunities arise for new species to form and coexist in communities. What sets an upper limit to specialization, thus setting an upper limit to speciation? We propose that MacArthur's theories of species packing and resource minimization may hold answers. Specifically, resources and individuals are finite-as species become increasingly specialized, each individual has fewer resources it can access. Species can only be as specialized as is possible in a given resource environment while still meeting basic resource requirements. We propose that the upper limit to specialization lies below the threshold that causes populations to be so small that stochastic extinctions take over, and that this limit is likely rarely approached due to the sequential timing by which new lineages arrive.

Spatial variability in plant predation determines the strength of stochastic community assembly.

High diversity is often poorly explained by trait-based deterministic models, in part because stochastic processes also influence community assembly. Testing how deterministic and stochastic processes combine to regulate diversity, however, has been limited by the spatial complexity of these interactions. Here, we demonstrate how spatial variability in small-mammal predation on plants, mostly by granivory, results in fine-scale switching between deterministically and stochastically regulated plant community assembly in an otherwise environmentally homogeneous tallgrass prairie. We initiated assembly with the uniform application of a 24-species mixture of prairie grasses and forbs, thereby setting the maximum level of diversity (γ-diversity). In field edges with higher densities of small mammals, traits reducing seed palatability deterministically produced homogeneous subsets of less palatable plant species within the first few months after planting (low α and ß diversity). As small-mammal densities decreased in more open areas, assembly unfolded stochastically on the basis of which planted species happened to land at a given location (high α and ß diversity). We used randomization models to validate that this higher ß diversity was explained by true differences in community structure among plots rather than by the hidden effects of increasing α diversity. The net effect at the site level was a spatially structured array of prairie species, including a positive relationship between diversity and environmental suitability relating to reduced predator intensity.

When Ecology Fails: How Reproductive Interactions Promote Species Coexistence.

That species must differ ecologically is often viewed as a fundamental condition for their stable coexistence in biological communities. Yet, recent work has shown that ecologically equivalent species can coexist when reproductive interactions and sexual selection regulate population growth. Here, we review theoretical models and highlight empirical studies supporting a role for reproductive interactions in maintaining species diversity. We place reproductive interactions research within a burgeoning conceptual framework of coexistence theory, identify four key mechanisms in intra- and interspecific interactions within and between sexes, speculate on novel mechanisms, and suggest future research. Given the preponderance of sexual reproduction in nature, our review suggests that this is a neglected path towards explaining species diversity when traditional ecological explanations have failed.

On the Origin of Coexisting Species.

Speciation is frequently initiated but rarely completed, a phenomenon hypothesized to arise due to the failure of nascent lineages to persist. Although a failure to persist often has ecological causes, key gaps exist between ecological and evolutionary theories that, if filled, would clarify when and why speciation succeeds or fails. Here, we apply ecological coexistence theory to show how the alignment between different forms of niche opportunity and niche use shape the initiation, progression, and completion of speciation. Niche evolution may drive coexistence or competitive exclusion, and an ability to coexist ecologically may help or hinder speciation. Our perspective allows progress towards unifying the origin and maintenance of species diversity across the tree of life.

Evolution of an inferior competitor increases resistance to biological invasion.

Biodiversity is imperilled by the spatial homogenization of life on Earth. As new species invade ecological communities, there is urgent need to understand when native species might resist or succumb to interactions with new species. In the California Floristic Province, a global biodiversity hotspot, we show that populations of a native grass (Vulpia microstachys) have evolved to resist the competitive impacts of a dominant European invader (Bromus hordeaceus). Contrary to classic theory, which predicts that competing species co-evolve to differentiate their niches, our evidence is instead most consistent with the native species having evolved to better compete for those resources used by the invader, curtailing the invader's spread. Evolution to resist an invader was achieved despite populations interacting within a diverse background community (22 species 0.5 m-2 on average), refuting the oft-cited hypothesis that high diversity precludes the evolution of pairwise species interactions. Lastly, unlike studies that have explored the demographic consequences of evolution under competition, ours does so with naturally evolved populations. Our study highlights evolution as an underappreciated coexistence mechanism, acting to buffer species from extinction in the face of biological invasion.

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.

Moving Character Displacement beyond Characters Using Contemporary Coexistence Theory.

Character displacement is one of the most studied phenomena in evolutionary biology, yet research has narrowly focused on demonstrating whether or not displacement has occurred. We propose a new experimental approach, adopted from the coexistence literature, that directly measures interspecific competition among sympatric and allopatric populations of species. Doing so allows increased ability to (i) test predictions of character displacement without biases inherent to character-centric tests, (ii) quantify its effect on the stability of coexistence, (iii) resolve the phenotypic pathways through which competitive divergence is achieved, and (iv) perform comparative tests. Our approach extends research to forms of character displacement not readily identified by past methods and will lead to a broader understanding of its consequences for community structure.