Tamara Münkemüller

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.

A road map for integrating eco-evolutionary processes into biodiversity models

The demand for projections of the future distribution of biodiversity has triggered an upsurge in modelling at the crossroads between ecology and evolution. Despite the enthusiasm around these so-called biodiversity models, most approaches are still criticised for not integrating key processes known to shape species ranges and community structure. Developing an integrative modelling framework for biodiversity distribution promises to improve the reliability of predictions and to give a better understanding of the eco-evolutionary dynamics of species and communities under changing environments. In this article, we briefly review some eco-evolutionary processes and interplays among them, which are essential to provide reliable projections of species distributions and community structure. We identify gaps in theory, quantitative knowledge and data availability hampering the development of an integrated modelling framework. We argue that model development relying on a strong theoretical foundation is essential to inspire new models, manage complexity and maintain tractability. We support our argument with an example of a novel integrated model for species distribution modelling, derived from metapopulation theory, which accounts for abiotic constraints, dispersal, biotic interactions and evolution under changing environmental conditions. We hope such a perspective will motivate exciting and novel research, and challenge others to improve on our proposed approach.

Functional species pool framework to test for biotic effects on community assembly

Functional trait differences among species are increasingly used to infer the effects of biotic and abiotic processes on species coexistence. Commonly, the trait diversity observed within communities is compared to patterns simulated in randomly generated communities based on sampling within a region. The resulting patterns of trait convergence and divergence are assumed to reveal abiotic and biotic processes, respectively. However, biotic processes such as competition can produce both trait divergence and convergence, through either excluding similar species (niche differences, divergence) or excluding dissimilar species (weaker competitor exclusion, convergence). Hence, separating biotic and abiotic processes that can produce identical patterns of trait diversity, or even patterns that neutralize each other, is not feasible with previous methods. We propose an operational framework in which the functional trait dissimilarity within communities (FDcomm) is compared to the corresponding trait dissimilarity expected from the species pool (i.e., functional species pool diversity, FDpool). FDpool includes the set of potential species for a site delimited by the operating environmental and dispersal limitation filters. By applying these filters, the resulting pattern of trait diversity is consistent with biotic processes, i.e., trait divergence (FDcomm > FDpool) indicates niche differentiation, while trait convergence (FDcomm < FDpool) indicates weaker competitor exclusion. To illustrate this framework, with its potential application and constraints, we analyzed both simulated and field data. The functional species pool framework more consistently detected the simulated trait diversity patterns than previous approaches. In the field, using data from plant communities of typical Northern European habitats in Estonia, we found that both niche-based and weaker competitor exclusion influenced community assembly, depending on the traits and community considered. In both simulated and field data, we demonstrated that only by estimating the species pool of a site is it possible to differentiate the patterns of trait dissimilarity produced by operating biotic processes. The framework, which can be applied with both functional and phylogenetic diversity, enables a reinterpretation of community assembly processes. Solving the challenge of defining an appropriate reference species pool for a site can provide a better understanding of community assembly.

The influence of interspecific interactions on species range expansion rates

Ongoing and predicted global change makes understanding and predicting species’ range shifts an urgent scientific priority. Here, we provide a synthetic perspective on the so far poorly understood effects of interspecific interactions on range expansion rates. We present theoretical foundations for how interspecific interactions may modulate range expansion rates, consider examples from empirical studies of biological invasions and natural range expansions as well as process-based simulations, and discuss how interspecific interactions can be more broadly represented in process-based, spatiotemporally explicit range forecasts. Theory tells us that interspecific interactions affect expansion rates via alteration of local population growth rates and spatial displacement rates, but also via effects on other demographic parameters. The best empirical evidence for interspecific effects on expansion rates comes from studies of biological invasions. Notably, invasion studies indicate that competitive dominance and release from specialized enemies can enhance expansion rates. Studies of natural range expansions especially point to the potential for competition from resident species to reduce expansion rates. Overall, it is clear that interspecific interactions may have important consequences for range dynamics, but also that their effects have received too little attention to robustly generalize on their importance. We then discuss how interspecific interactions effects can be more widely incorporated in dynamic modeling of range expansions. Importantly, models must describe spatiotemporal variation in both local population dynamics and dispersal. Finally, we derive the following guidelines for when it is particularly important to explicitly represent interspecific interactions in dynamic range expansion forecasts: if most interacting species show correlated spatial or temporal trends in their effects on the target species, if the number of interacting species is low, and if the abundance of one or more strongly interacting species is not closely linked to the abundance of the target species.

Phylogenetic niche conservatism – common pitfalls and ways forward

1. The prevalence of phylogenetic niche conservatism (PNC) in nature is still a conflicting issue. Disagreement arises from confusion over its precise definition and the variety of approaches to measure its prevalence. Recent work highlighted that common measures of PNC strongly depend on the assumptions of the underlying model of niche evolution. However, this warning has not been well recognized in the applied literature and questionable approaches are still frequently applied. 2. The aim of this paper is to draw attention to the assumptions underlying commonly applied simple measures of PNC. We used a series of simulations to illustrate how misleading results can be if assumptions of niche evolution are violated, that the violation of assumptions is a common phenomenon and that testing assumptions requires in-depth pre-test. 3. We conclude that the seemingly simple measures of PNC, such as phylogenetic sign6al and evolutionary rate, are not so easy to apply if one accounts for the necessity to test model assumptions. In addition, these measures can be difficult to interpret. The common assumption that strong phylogenetic signal indicates PNC will be often invalid. In addition, the interpretation of some measures, e.g. the conclusion that evolutionary rate is slow enough to indicate PNC, requires a comparison with another clade, another trait or well-developed null model assumptions and thus additional data. 4. We suggest that studies investigating PNC should always compare alternative evolutionary models, and that model comparisons should in particular include flexible niche evolution models such as multiple-optima OU models, although these are computational intensive. These models are directly inherited from the concept of macro-evolutionary adaptive landscape, and can indicate PNC either by relative few peak shifts or by narrow peaks in the adaptive landscape. A test of PNC thus requires comparing these parameters of the macroevolutionary landscape between clades or time periods. 5. The general prevalence of PNC in nature should be evaluated only based on studies keeping up to the high standards of communicating the used definition of PNC, testing the assumptions made in the modelling approaches and including newly developed models in a model comparison approach.

Density-regulated population dynamics and conditional dispersal alter the fate of mutations occurring at the front of an expanding population

There is an increasing recognition that the interplay between ecological and evolutionary processes shapes the genetic footprint of populations during and after range expansions. However, more complex ecological processes regularly considered within spatial ecology remain unexplored in models describing the population genetics of range expansion. In this study we integrate flexible descriptions of population growth and competition as well as conditional dispersal into a model that simulates the fate of mutations occurring at the wave front of an expanding population. Our results show that the survival and distribution of a mutation is not only affected by its bias (that is, whether it is deleterious, neutral or beneficial) but also by the mode of local density regulation and conditional dispersal of the simulated populations. It is in particular the chance of a mutation to establish at the front of advance and ‘surf’ to high frequencies that critically depends on the investigated ecological processes. This is because of the influence of these processes on demographic stochasticity in the system and the differential responses of deleterious, neutral and beneficial mutations to this stochasticity. Generally, deleterious mutations rely more on chance and thus profit the most from ecological processes that enhance demographic stochasticity during the period of establishment. Our study emphasizes the importance of incorporating more ecological realism into evolutionary models to better understand the consequences of shifting geographic ranges for the genetic structure of populations and to find efficient adaptation strategies to mitigate these effects.

Spatial scale and intraspecific trait variability mediate assembly rules in alpine grasslands

Summary 1.Assembly of grassland communities has long been scrutinized through the lens of functional diversity. Studies generally point to an overwhelming influence of climate on observed patterns of functional diversity, despite experimental evidence demonstrating the importance of biotic interactions. We postulate that this is because most observational studies neglect both scale-dependencies of assembly processes and phenotypic variation between individuals. Here, we test for changes in the importance of abiotic filtering and biotic interactions along a stress gradient by explicitly accounting for different scales. In addition to quantifying intraspecific trait variability, we also vary the two components of spatial scale, including grain (i.e. community size) and extent (i.e. the geographic area that defines the species pool). 2.We sampled twenty grassland communities in ten sites distributed along a 975 m elevation gradient. At each site, we measured seven functional traits for a total of 2,020 individuals at different spatial grains. We related community functional diversity metrics to the main environmental gradient of our study area, growing season length, and assessed the dependence of these relationships on spatial grain, spatial extent and intraspecific trait variability. 3.At large spatial grain and extent, the imprint of environmental filtering on functional diversity became more important with increasing stress (i.e. functional diversity decreased with shorter growing season length). At small spatial grain and extent we found a convex relationship between functional diversity and growing season length congruent with the hypothesis that competition is dominant at low stress levels while facilitative interactions are dominant at high stress levels (i.e. high functional diversity at both extremes of the stress gradient). Importantly, the effect of intraspecific variability on assembly rules was noticeable only at small spatial grain and extent. 4.Synthesis. Our study reveals how the combination of abiotic stress and biotic interactions shape the functional diversity of alpine grasslands at different spatial scales, and highlights the importance of phenotype variation between individuals for community assembly processes at fine spatial scale. Our results suggest that studies analysing trait-based assembly rules but ignoring intraspecific trait variability and focusing on a single spatial scale are likely to miss essential features of community diversity patterns. This article is protected by copyright. All rights reserved.

N-dimensional hypervolumes to study stability of complex ecosystems.

Although our knowledge on the stabilising role of biodiversity and on how it is affected by perturbations has greatly improved, we still lack a comprehensive view on ecosystem stability that is transversal to different habitats and perturbations. Hence, we propose a framework that takes advantage of the multiplicity of components of an ecosystem and their contribution to stability. Ecosystem components can range from species or functional groups, to different functional traits, or even the cover of different habitats in a landscape mosaic. We make use of n-dimensional hypervolumes to define ecosystem states and assess how much they shift after environmental changes have occurred. We demonstrate the value of this framework with a study case on the effects of environmental change on Alpine ecosystems. Our results highlight the importance of a multidimensional approach when studying ecosystem stability and show that our framework is flexible enough to be applied to different types of ecosystem components, which can have important implications for the study of ecosystem stability and transient dynamics.

Identifying the signal of environmental filtering and competition in invasion patterns – a contest of approaches from community ecology

Summary In 1859, Darwin had already identified environmental constraints and competition with the native community as major drivers of invasion success. Since then, a toolbox of indices and statistical approaches has been developed and commonly applied to test for the relative importance of these drivers. This toolbox is largely based on community ecology theory with the underlying hypothesis that patterns of trait (or phylogenetic) similarities between invaders and native species permit to disentangle the signatures of competition and environmental filtering. However, so far the performance of the indices and statistical approaches has not been thoroughly evaluated, and there exists no study exploring the sensitivity of the different methods given common biases in field data. This severely hampers intercomparisons of invasion studies and ultimately prevents the elaboration of general conclusions. In this study, we developed a mechanistic community assembly model to simulate invasion patterns across a range of communities and tested the performance of four different indices aiming at disentangling environmental filtering vs. competition from these patterns. Furthermore, we evaluated the sensitivity of the statistical methods to biases in the data (resulting from non-equilibrium dynamics or observation errors). Our results indicated that the best performing index was mean distance to the native species (the average functional distance between the invader and all the species of the community), especially in heterogeneous landscapes. Further, we demonstrated that the detection of competition was more sensitive to the presence of biases in the data than the detection of environmental filtering. In conclusion, studying invasion mechanisms based on community patterns is possible when employing the appropriate statistical method, but it is highly sensitive to the quality of the data set used.

Extreme climate events counteract the effects of climate and land‐use changes in Alpine tree lines

1. Climate change and extreme events, such as drought, threaten ecosystems worldwide and in particular mountain ecosystems, where species often live at their environmental tolerance limits. In the European Alps, plant communities are also influenced by land-use abandonment leading to woody encroachment of subalpine and alpine grasslands. 2. In this study, we explored how the forest-grassland ecotone of Alpine treelines will respond to gradual climate warming, drought events and land-use change in terms of forest expansion rates, taxonomic diversity and functional composition. We used a previously validated dynamic vegetation model, FATE-HD, parameterised for plant communities in the Ecrins National Park in the French Alps. 3. Our results showed that intense drought counteracted the forest expansion at higher elevations driven by land-use abandonment and climate change, especially when combined with high drought frequency (occurring every 2 or less than 2 years). 4. Furthermore, intense and frequent drought accelerated the rates of taxonomic change and resulted in overall higher taxonomic spatial heterogeneity of the ecotone than would be expected under gradual climate and land-use changes only. 5. Synthesis and applications. The results from our model show that intense and frequent drought counteracts forest expansion driven by climate and land-use changes in the forest-grassland ecotone of Alpine treelines. We argue that land-use planning must consider the effects of extreme events, such as drought, as well as climate and land-use changes, since extreme events might interfere with trends predicted under gradual climate warming and agricultural abandonment.