Rudolf P. Rohr

Ecophylogenetics: advances and perspectives

Ecophylogenetics can be viewed as an emerging fusion of ecology, biogeography and macroevolution. This new and fast‐growing field is promoting the incorporation of evolution and historical contingencies into the ecological research agenda through the widespread use of phylogenetic data. Including phylogeny into ecological thinking represents an opportunity for biologists from different fields to collaborate and has provided promising avenues of research in both theoretical and empirical ecology, towards a better understanding of the assembly of communities, the functioning of ecosystems and their responses to environmental changes. The time is ripe to assess critically the extent to which the integration of phylogeny into these different fields of ecology has delivered on its promise. Here we review how phylogenetic information has been used to identify better the key components of species interactions with their biotic and abiotic environments, to determine the relationships between diversity and ecosystem functioning and ultimately to establish good management practices to protect overall biodiversity in the face of global change. We evaluate the relevance of information provided by phylogenies to ecologists, highlighting current potential weaknesses and needs for future developments. We suggest that despite the strong progress that has been made, a consistent unified framework is still missing to link local ecological dynamics to macroevolution. This is a necessary step in order to interpret observed phylogenetic patterns in a wider ecological context. Beyond the fundamental question of how evolutionary history contributes to shape communities, ecophylogenetics will help ecology to become a better integrative and predictive science.

On the structural stability of mutualistic systems

Introduction Several major developments in theoretical ecology have relied on either dynamical stability or numerical simulations, but oftentimes, they have found contradictory results. This is partly a result of not rigorously checking either the assumption that a steady state is feasible—meaning, all species have constant and positive abundances—or the dependence of results to model parameterization. Here, we extend the concept of structural stability to community ecology in order to account for these two problems. Specifically, we studied the set of conditions leading to the stable coexistence of all species within a community. This shifts the question from asking whether we can find a feasible equilibrium point for a fixed set of parameter values, to asking how large is the range of parameter values that are compatible with the stable coexistence of all species. The architecture of plant-animal mutualistic networks modulates the range of conditions leading to the stable coexistence of all species. The area of the different domains represents the structural stability of a model of mutualistic communities with a given network architecture. The nested networks observed in nature—illustrated here by the network at the bottom—lead to a maximum structural stability. Rationale We begin by disentangling the conditions of global stability from the conditions of feasibility of a steady state in ecological systems. To quantify the domain of stable coexistence, we first find its center (the structural vector of intrinsic growth rates). Next, we determine the boundaries of such a domain by quantifying the amount of variation from the structural vector tolerated before one species goes extinct. Through this two-step approach, we disentangle the effects of the size of the feasibility domain from how close a solution is to its boundary, which is at the heart of previous contradictory results. We illustrate our method by exploring how the observed architecture of mutualistic networks between plants and their pollinators or seed dispersers affects their domain of stable coexistence. Results First, we determined the network architecture that maximizes the structural stability of mutualistic systems. This corresponds to networks with a maximal level of nestedness, a small trade-off between the number and intensity of interactions a species has, and a high level of mutualistic strength within the constraints of global stability. Second, we found that the large majority of observed mutualistic networks are close to this optimum network architecture, maximizing the range of parameters that are compatible with species coexistence. Conclusion Structural stability has played a major role in several fields such as evolutionary developmental biology, in which it has brought the view that some morphological structures are more common than others because they are compatible with a wider range of developmental conditions. In community ecology, structural stability is the sort of framework needed to study the consequences of global environmental change—by definition, large and directional—on species coexistence. Structural stability will serve to assess both the range of variability a given community can withstand and why some community patterns are more widespread than others. A structural approach to species interactions What determines the stability of ecological networks? Rohr et al. devised a conceptual approach to study interactions between species that emphasizes the role of network structure (see the Perspective by Pawar). Using the example of mutualistic networks of communities of plants and their pollinator species, they show how the structure of networks can determine the persistence of the interactions. Network structures and architectures observed in nature intrinsically match the most stable solution. This approach has promise for application to questions of ecological community stability under global change. Science, this issue 10.1126/science.1253497; see also p. 383 In ecology, structural stability influences the range of perturbations mutualistic networks can withstand. [Also see Perspective by Pawar] In theoretical ecology, traditional studies based on dynamical stability and numerical simulations have not found a unified answer to the effect of network architecture on community persistence. Here, we introduce a mathematical framework based on the concept of structural stability to explain such a disparity of results. We investigated the range of conditions necessary for the stable coexistence of all species in mutualistic systems. We show that the apparently contradictory conclusions reached by previous studies arise as a consequence of overseeing either the necessary conditions for persistence or its dependence on model parameterization. We show that observed network architectures maximize the range of conditions for species coexistence. We discuss the applicability of structural stability to study other types of interspecific interactions.

Modeling Food Webs: Exploring Unexplained Structure Using Latent Traits

Several stochastic models have tried to capture the architecture of food webs. This approach is interesting, but it is limited by the fact that different assumptions can yield similar results. To overcome this limitation, we develop a purely statistical approach. Body size in terms of an optimal ratio between prey and predator is used as explanatory variable. In 12 observed food webs, this model predicts, on average, 20% of interactions. To analyze the unexplained part, we introduce a latent term: each species is described by two latent traits, foraging and vulnerability, that represent nonmeasured characteristics of species once the optimal body size has been accounted for. The model now correctly predicts an average of 73% of links. The key features of our approach are that latent traits quantify the structure that is left unexplained by the explanatory variable and that this quantification allows a test of whether independent biological information, such as microhabitat use, camouflage, or phylogeny, explains this structure. We illustrate this method with phylogeny and find that it is linked to one or both latent traits in nine of 12 food webs. Our approach opens the door to the formulation of more complex models that can be applied to any kind of biological network.

Alien plant species with a wider global distribution are better able to capitalize on increased resource availability

• A high ability of alien plant species to capitalize on increases in resource availability has been suggested as an explanation for being globally successful. Here, we tested this hypothesis meta-analytically using existing data from experiments manipulating plant resources (light, water and nutrients). • From these studies we extracted the response to resource increase of biomass, as an indicator of plant performance, and the responses of two traits related to resource capture: root : shoot ratio and specific leaf area (SLA). For 211 species recorded in the Global Compendium of Weeds, we assessed the relationship between effect sizes from such studies and the number of global regions where a species was established. • We found that globally widespread species exhibited greater biomass responses to increases in resources overall, compared to less widespread species. Root : shoot ratio and SLA responses to increased resource availability were not related to species global distribution. • In general, globally widespread alien plant species were better able to capitalize on increased availability of resources, through achieving increased growth and biomass accumulation, while greater plasticity of key resource-capture traits per se did not appear to be related to greater success.

Determinants of plant establishment success in a multispecies introduction experiment with native and alien species

Determinants of plant establishment and invasion are a key issue in ecology and evolution. Although establishment success varies substantially among species, the importance of species traits and extrinsic factors as determinants of establishment in existing communities has remained difficult to prove in observational studies because they can be confounded and mask each other. Therefore, we conducted a large multispecies field experiment to disentangle the relative importance of extrinsic factors vs. species characteristics for the establishment success of plants in grasslands. We introduced 48 alien and 45 native plant species at different seed numbers into multiple grassland sites with or without experimental soil disturbance and related their establishment success to species traits assessed in five independent multispecies greenhouse experiments. High propagule pressure and high seed mass were the most important factors increasing establishment success in the very beginning of the experiment. However, after 3 y, propagule pressure became less important, and species traits related to biotic interactions (including herbivore resistance and responses to shading and competition) became the most important drivers of success or failure. The relative importance of different traits was environment-dependent and changed over time. Our approach of combining a multispecies introduction experiment in the field with trait data from independent multispecies experiments in the greenhouse allowed us to detect the relative importance of species traits for early establishment and provided evidence that species traits—fine-tuned by environmental factors—determine success or failure of alien and native plants in temperate grasslands.

Anthropogenic disturbance as a driver of microspatial and microhabitat segregation of cytotypes of Centaurea stoebe and cytotype interactions in secondary contact zones

BACKGROUND AND AIMS In a mixed-ploidy population, strong frequency-dependent mating will lead to the elimination of the less common cytotype, unless prezygotic barriers enhance assortative mating. However, such barriers favouring cytotype coexistence have only rarely been explored. Here, an assessment is made of the mechanisms involved in formation of mixed-ploidy populations and coexistence of diploid plants and their closely related allotetraploid derivates from the Centaurea stoebe complex (Asteraceae). METHODS An investigation was made of microspatial and microhabitat distribution, life-history and fitness traits, flowering phenology, genetic relatedness of cytotypes and intercytotype gene flow (cpDNA and microsatellites) in six mixed-ploidy populations in Central Europe. KEY RESULTS Diploids and tetraploids were genetically differentiated, thus corroborating the secondary origin of contact zones. The cytotypes were spatially segregated at all sites studied, with tetraploids colonizing preferentially drier and open microhabitats created by human-induced disturbances. Conversely, they were rare in more natural microsites and microsites with denser vegetation despite their superior persistence ability (polycarpic life cycle). The seed set of tetraploid plants was strongly influenced by their frequency in mixed-ploidy populations. Triploid hybrids originated from bidirectional hybridizations were extremely rare and almost completely sterile, indicating a strong postzygotic barrier between cytotypes. CONCLUSIONS The findings suggest that tetraploids are later immigrants into already established diploid populations and that anthropogenic activities creating open niches favouring propagule introductions were the major factor shaping the non-random distribution and habitat segregation of cytotypes at fine spatial scale. Establishment and spread of tetraploids was further facilitated by their superior persistence through the perennial life cycle. The results highlight the importance of non-adaptive spatio-temporal processes in explaining microhabitat and microspatial segregation of cytotypes.

Phylogeny versus body size as determinants of food web structure

Food webs are the complex networks of trophic interactions that stoke the metabolic fires of life. To understand what structures these interactions in natural communities, ecologists have developed simple models to capture their main architectural features. However, apparently realistic food webs can be generated by models invoking either predator–prey body-size hierarchies or evolutionary constraints as structuring mechanisms. As a result, this approach has not conclusively revealed which factors are the most important. Here we cut to the heart of this debate by directly comparing the influence of phylogeny and body size on food web architecture. Using data from 13 food webs compiled by direct observation, we confirm the importance of both factors. Nevertheless, phylogeny dominates in most networks. Moreover, path analysis reveals that the size-independent direct effect of phylogeny on trophic structure typically outweighs the indirect effect that could be captured by considering body size alone. Furthermore, the phylogenetic signal is asymmetric: closely related species overlap in their set of consumers far more than in their set of resources. This is at odds with several food web models, which take only the view-point of consumers when assigning interactions. The echo of evolutionary history clearly resonates through current food webs, with implications for our theoretical models and conservation priorities.

The importance of landscape and spatial structure for hymenopteran-based food webs in an agro-ecosystem

1. Understanding the environmental factors that structure biodiversity and food webs among communities is central to assess and mitigate the impact of landscape changes. 2. Wildflower strips are ecological compensation areas established in farmland to increase pollination services and biological control of crop pests and to conserve insect diversity. They are arranged in networks in order to favour high species richness and abundance of the fauna. 3. We describe results from experimental wildflower strips in a fragmented agricultural landscape, comparing the importance of landscape, of spatial arrangement and of vegetation on the diversity and abundance of trap-nesting bees, wasps and their enemies, and the structure of their food webs. 4. The proportion of forest cover close to the wildflower strips and the landscape heterogeneity stood out as the most influential landscape elements, resulting in a more complex trap-nest community with higher abundance and richness of hosts, and with more links between species in the food webs and a higher diversity of interactions. We disentangled the underlying mechanisms for variation in these quantitative food web metrics. 5. We conclude that in order to increase the diversity and abundance of pollinators and biological control agents and to favour a potentially stable community of cavity-nesting hymenoptera in wildflower strips, more investment is needed in the conservation and establishment of forest habitats within agro-ecosystems, as a reservoir of beneficial insect populations.

Selection on stability across ecological scales

Much of the focus in evolutionary biology has been on the adaptive differentiation among organisms. It is equally important to understand the processes that result in similarities of structure among systems. Here, we discuss examples of similarities occurring at different ecological scales, from predator-prey relations (attack rates and handling times) through communities (food-web structures) to ecosystem properties. Selection among systemic configurations or patterns that differ in their intrinsic stability should lead generally to increased representation of relatively stable structures. Such nonadaptive, but selective processes that shape ecological communities offer an enticing mechanism for generating widely observed similarities, and have sparked new interest in stability properties. This nonadaptive systemic selection operates not in opposition to, but in parallel with, adaptive evolution.

Combining food web and species distribution models for improved community projections.

The ability to model biodiversity patterns is of prime importance in this era of severe environmental crisis. Species assemblage along environmental gradients is subject to the interplay of biotic interactions in complement to abiotic filtering and stochastic forces. Accounting for complex biotic interactions for a wide array of species remains so far challenging. Here, we propose using food web models that can infer the potential interaction links between species as a constraint in species distribution models. Using a plant–herbivore (butterfly) interaction dataset, we demonstrate that this combined approach is able to improve species distribution and community forecasts. The trophic interaction network between butterfly larvae and host plant was phylogenetically structured and driven by host plant nitrogen content allowing forecasting the food web model to unknown interactions links. This combined approach is very useful in rendering models of more generalist species that have multiple potential interaction links, where gap in the literature may occur. Our combined approach points toward a promising direction for modeling the spatial variation in entire species interaction networks.