Phenotypic plasticity and the effects of thermal fluctuations on specialists and generalists.

Classical theories predict that relatively constant environments should generally favour specialists, while fluctuating environments should be selected for generalists. However, theoretical and empirical results have pointed out that generalist organisms might, on the contrary, perform poorly under fluctuations. In particular, if generalism is underlaid by phenotypic plasticity, performance of generalists should be modulated by the temporal characteristics of environmental fluctuations. Here, we used experiments in microcosms of Tetrahymena thermophila ciliates and a mathematical model to test whether the period or autocorrelation of thermal fluctuations mediate links between the level of generalism and the performance of organisms under fluctuations. In the experiment, thermal fluctuations consistently impeded performance compared with constant conditions. However, the intensity of this effect depended on the level of generalism: while the more specialist strains performed better under fast or negatively autocorrelated fluctuations, plastic generalists performed better under slow or positively autocorrelated fluctuations. Our model suggests that these effects of fluctuations on organisms' performance may result from a time delay in the expression of plasticity, restricting its benefits to slow enough fluctuations. This study points out the need to further investigate the temporal dynamics of phenotypic plasticity to better predict its fitness consequences under environmental fluctuations.

The Phylogenetic Limits to Diversity-Dependent Diversification.

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence each other's diversification? In other words: are there phylogenetic limits to this diversity-dependence? Islands form ideal systems to answer these questions because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, i.e., all mainland species can colonize and diversify independently from one another. We term this clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all island species of a taxonomic group regardless of their mainland ancestry, i.e., diversity-dependence applies both to species within the same clade and between different clades established by different mainland species. We call this island-wide (IW) diversity-dependence. We present a method to compute a likelihood for this model given phylogenetic data on colonization and branching events and use likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes that are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e., IW diversity-dependence. But it could also be suggestive of only within-clade interactions because between-clade interactions would have blocked the same ecotype from re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to diversity-dependent diversification. We discuss possibilities for future extensions and applications of our modelling approach. [Adaptive radiation; birth-death model; Caribbean; diversity-dependence; Eleutherodactylus; island biogeography.].

Phytoplankton biodiversity is more important for ecosystem functioning in highly variable thermal environments.

The 21st century has seen an acceleration of anthropogenic climate change and biodiversity loss, with both stressors deemed to affect ecosystem functioning. However, we know little about the interactive effects of both stressors and in particular about the interaction of increased climatic variability and biodiversity loss on ecosystem functioning. This should be remedied because larger climatic variability is one of the main features of climate change. Here, we demonstrated that temperature fluctuations led to changes in the importance of biodiversity for ecosystem functioning. We used microcosm communities of different phytoplankton species richness and exposed them to a constant, mild, and severe temperature-fluctuating environment. Wider temperature fluctuations led to steeper biodiversity-ecosystem functioning slopes, meaning that species loss had a stronger negative effect on ecosystem functioning in more fluctuating environments. For severe temperature fluctuations, the slope increased through time due to a decrease of the productivity of species-poor communities over time. We developed a theoretical competition model to better understand our experimental results and showed that larger differences in thermal tolerances across species led to steeper biodiversity-ecosystem functioning slopes. Species-rich communities maintained their ecosystem functioning with increased fluctuation as they contained species able to resist the thermally fluctuating environments, while this was on average not the case in species-poor communities. Our results highlight the importance of biodiversity for maintaining ecosystem functions and services in the context of increased climatic variability under climate change.

Spatial heterogeneity of biomass turnover has contrasting effects on synchrony and stability in trophic metacommunities.

Spatial heterogeneity is a fundamental feature of ecosystems, and ecologists have identified it as a factor promoting the stability of population dynamics. In particular, differences in interaction strengths and resource supply between patches generate an asymmetry of biomass turnover with a fast and a slow patch coupled by a mobile predator. Here, we demonstrate that asymmetry leads to opposite stability patterns in metacommunities receiving localized perturbations depending on the characteristics of the perturbed patch. Perturbing prey in the fast patch synchronizes the dynamics of prey biomass between the two patches and destabilizes predator dynamics by increasing the predator's temporal variability. Conversely, perturbing prey in the slow patch decreases the synchrony of the prey's dynamics and stabilizes predator dynamics. Our results have implications for conservation ecology and suggest reinforcing protection policies in fast patches to dampen the effects of perturbations and promote the stability of population dynamics at the regional scale.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

Detecting Lineage-Specific Shifts in Diversification: A Proper Likelihood Approach.

The branching patterns of molecular phylogenies are generally assumed to contain information on rates of the underlying speciation and extinction processes. Simple birth-death models with constant, time-varying, or diversity-dependent rates have been invoked to explain these patterns. They have one assumption in common: all lineages have the same set of diversification rates at a given point in time. It seems likely, however, that there is variability in diversification rates across subclades in a phylogenetic tree. This has inspired the construction of models that allow multiple rate regimes across the phylogeny, with instantaneous shifts between these regimes. Several methods exist for calculating the likelihood of a phylogeny under a specified mapping of diversification regimes and for performing inference on the most likely diversification history that gave rise to a particular phylogenetic tree. Here, we show that the likelihood computation of these methods is not correct. We provide a new framework to compute the likelihood correctly and show, with simulations of a single shift, that the correct likelihood indeed leads to parameter estimates that are on average in much better agreement with the generating parameters than the incorrect likelihood. Moreover, we show that our corrected likelihood can be extended to multiple rate shifts in time-dependent and diversity-dependent models. We argue that identifying shifts in diversification rates is a nontrivial model selection exercise where one has to choose whether shifts in now-extinct lineages are taken into account or not. Hence, our framework also resolves the recent debate on such unobserved shifts. [Diversification; macroevolution; phylogeny; speciation].

Theory of temperature-dependent consumer-resource interactions.

Changes in temperature affect consumer-resource interactions, which underpin the functioning of ecosystems. However, existing studies report contrasting predictions regarding the impacts of warming on biological rates and community dynamics. To improve prediction accuracy and comparability, we develop an approach that combines sensitivity analysis and aggregate parameters. The former determines which biological parameters impact the community most strongly. The use of aggregate parameters (i.e., maximal energetic efficiency, ρ, and interaction strength, κ), that combine multiple biological parameters, increases explanatory power and reduces the complexity of theoretical analyses. We illustrate the approach using empirically derived thermal dependence curves of biological rates and applying it to consumer-resource biomass ratio and community stability. Based on our analyses, we generate four predictions: (1) resource growth rate regulates biomass distributions at mild temperatures, (2) interaction strength alone determines the thermal boundaries of the community, (3) warming destabilises dynamics at low and mild temperatures only and (4) interactions strength must decrease faster than maximal energetic efficiency for warming to stabilise dynamics. We argue for the potential benefits of directly working with the aggregate parameters to increase the accuracy of predictions on warming impacts on food webs and promote cross-system comparisons.

Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists.

Limited dispersal is classically considered as a prerequisite for ecological specialization to evolve, such that generalists are expected to show greater dispersal propensity compared with specialists. However, when individuals choose habitats that maximize their performance instead of dispersing randomly, theory predicts dispersal with habitat choice to evolve in specialists, while generalists should disperse more randomly. We tested whether habitat choice is associated with thermal niche specialization using microcosms of the ciliate Tetrahymena thermophila, a species that performs active dispersal. We found that thermal specialists preferred optimal habitats as predicted by theory, a link that should make specialists more likely to track suitable conditions under environmental changes than expected under the random dispersal assumption. Surprisingly, generalists also performed habitat choice but with a preference for suboptimal habitats. Since this result challenges current theory, we developed a metapopulation model to understand under which circumstances such a preference for suboptimal habitats should evolve. We showed that competition between generalists and specialists may favor a preference for niche margins in generalists under environmental variability. Our results demonstrate that the behavioral dimension of dispersal-here, habitat choice-fundamentally alters our predictions of how dispersal evolve with niche specialization, making dispersal behaviors crucial for ecological forecasting facing environmental changes.

Additional Analytical Support for a New Method to Compute the Likelihood of Diversification Models.

Molecular phylogenies have been increasingly recognized as an important source of information on species diversification. For many models of macroevolution, analytical likelihood formulas have been derived to infer macroevolutionary parameters from phylogenies. A few years ago, a general framework to numerically compute such likelihood formulas was proposed, which accommodates models that allow speciation and/or extinction rates to depend on diversity. This framework calculates the likelihood as the probability of the diversification process being consistent with the phylogeny from the root to the tips. However, while some readers found the framework presented in Etienne et al. (Proc R Soc Lond B Biol Sci 279(1732):1300-1309, 2012) convincing, others still questioned it (personal communication), despite numerical evidence that for special cases the framework yields the same (i.e., within double precision) numerical value for the likelihood as analytical formulas do that were independently derived for these special cases. Here we prove analytically that the likelihoods calculated in the new framework are correct for all special cases with known analytical likelihood formula. Our results thus add substantial mathematical support for the overall coherence of the general framework.

The inherent multidimensionality of temporal variability: how common and rare species shape stability patterns.

Empirical knowledge of diversity-stability relationships is mostly based on the analysis of temporal variability. Variability, however, often depends on external factors that act as disturbances, which makes comparisons across systems difficult to interpret. Here, we show how variability can reveal inherent stability properties of ecological communities. This requires that we abandon one-dimensional representations, in which a single variability measurement is taken as a proxy for how stable a system is, and instead consider the whole set of variability values generated by all possible stochastic perturbations. Despite this complexity, in species-rich systems, a generic pattern emerges from community assembly, relating variability to the abundance of perturbed species. Strikingly, the contrasting contributions of different species abundance classes to variability, driven by different types of perturbations, can lead to opposite diversity-stability patterns. We conclude that a multidimensional perspective on variability helps reveal the dynamical richness of ecological systems and the underlying meaning of their stability patterns.

Trade-offs in the provisioning and stability of ecosystem services in agroecosystems.

Changes in land use generate trade-offs in the delivery of ecosystem services in agricultural landscapes. However, we know little about how the stability of ecosystem services responds to landscape composition, and what ecological mechanisms underlie these trade-offs. Here, we develop a model to investigate the dynamics of three ecosystem services in intensively managed agroecosystems, i.e., pollination-independent crop yield, crop pollination, and biodiversity. Our model reveals trade-offs and synergies imposed by landscape composition that affect not only the magnitude but also the stability of ecosystem service delivery. Trade-offs involving crop pollination are strongly affected by the degree to which crops depend on pollination and by their relative requirement for pollinator densities. We show conditions for crop production to increase with biodiversity and decreasing crop area, reconciling farmers' profitability and biodiversity conservation. Our results further suggest that, for pollination-dependent crops, management strategies that focus on maximizing yield will often overlook its stability. Given that agriculture has become more pollination-dependent over time, it is essential to understand the mechanisms driving these trade-offs to ensure food security.

The relationship between the spatial scaling of biodiversity and ecosystem stability.

AIM: Ecosystem stability and its link with biodiversity have mainly been studied at the local scale. Here we present a simple theoretical model to address the joint dependence of diversity and stability on spatial scale, from local to continental. METHODS: The notion of stability we use is based on the temporal variability of an ecosystem-level property, such as primary productivity. In this way, our model integrates the well-known species-area relationship (SAR) with a recent proposal to quantify the spatial scaling of stability, called the invariability-area relationship (IAR). RESULTS: We show that the link between the two relationships strongly depends on whether the temporal fluctuations of the ecosystem property of interest are more correlated within than between species. If fluctuations are correlated within species but not between them, then the IAR is strongly constrained by the SAR. If instead individual fluctuations are only correlated by spatial proximity, then the IAR is unrelated to the SAR. We apply these two correlation assumptions to explore the effects of species loss and habitat destruction on stability, and find a rich variety of multi-scale spatial dependencies, with marked differences between the two assumptions. MAIN CONCLUSIONS: The dependence of ecosystem stability on biodiversity across spatial scales is governed by the spatial decay of correlations within and between species. Our work provides a point of reference for mechanistic models and data analyses. More generally, it illustrates the relevance of macroecology for ecosystem functioning and stability.

A graphical-mechanistic approach to spatial resource competition.

Ecological communities are structured by processes operating at multiple spatial scales, which results in an often daunting complexity. Here we present a simple graphical theory to study the interaction of two fundamental community processes: resource competition at the local scale and dispersal at the regional scale. We consider a metacommunity model with two habitat patches in which consumer species compete for a spatially distributed resource. We introduce a graphical construction of the equilibrium metacommunity composition, analogous to traditional competition theory for two resources. As in the nonspatial case, the zero net growth isoclines (ZNGIs) play a central role in the analysis. We show that a consumer species' ZNGI depends on its dispersal characteristics, and this dependence leads to a unification of various dispersal-based coexistence mechanisms. We illustrate this unification using four specific mechanisms: species-specific dispersal rates, spatially asymmetric dispersal, resource-dependent dispersal, and competition between habitat specialists and generalists.

Long-Distance Rescue and Slow Extinction Dynamics Govern Multiscale Metapopulations.

Rare long-distance dispersal is known to be critical for species dynamics, but how the interplay between short- and long-distance colonization influences regional persistence in a fragmented habitat remains poorly understood. We propose a metapopulation model that combines local colonization within habitat islands and long-distance colonization between islands. We study how regional occupancy dynamics are affected by the multiscale colonization process. We find that the island size distribution (ISD) is a key driver of the long-term occupancy dynamics. When the ISD is heterogeneous-that is, when the size of islands is variable-we show that extinction dynamics become very slow. We demonstrate that this behavior is unrelated to the well-known extinction debt near the critical extinction threshold. Hence, this finding questions the equivalence between extinction debt and critical transitions in the context of metapopulation collapse. Furthermore, we show that long-distance colonization can rescue small islands from extinction and sustain a steady regional occupancy. These results provide novel theoretical and practical insights into extinction dynamics and persistence in fragmented habitats and are thus relevant for the design of conservation strategies.

A sampling formula for ecological communities with multiple dispersal syndromes.

Over the past decade, the neutral theory of biodiversity has stirred up community assembly theory considerably by suggesting that stochasticity in the form of ecological drift is an important factor determining community composition and community turnover. The neutral theory assumes that all species within a community are functionally equivalent (the neutrality assumption), and therefore applies best to communities of trophically similar species. Evidently, trophically similar species may still differ in dispersal ability, and therefore may not be completely functionally equivalent. Here we present a new sampling formula that takes into account the partitioning of a community into two guilds that differ in immigration rate. We show that, using this sampling formula, we can accurately detect a subdivision into guilds from species abundance distributions, given ecological data about dispersal ability. We apply our sampling formula to tropical tree data from Barro Colorado Island, Panama. Tropical trees are divided depending on their dispersal mode, where biotically dispersed trees are grouped as one guild, and abiotically dispersed trees represent another guild. We find that breaking neutrality by adding guild structure to the neutral model significantly improves the fit to data and provides a better understanding of community assembly on BCI. Our findings are thus an important step towards an integration of neutral and niche theory.

General relationships between consumer dispersal, resource dispersal and metacommunity diversity.

One of the central questions of metacommunity theory is how dispersal of organisms affects species diversity. Here, we show that the diversity-dispersal relationship should not be studied in isolation of other abiotic and biotic flows in the metacommunity. We study a mechanistic metacommunity model in which consumer species compete for an abiotic or biotic resource. We consider both consumer species specialised to a habitat patch, and generalist species capable of using the resource throughout the metacommunity. We present analytical results for different limiting values of consumer dispersal and resource dispersal, and complement these results with simulations for intermediate dispersal values. Our analysis reveals generic patterns for the combined effects of consumer and resource dispersal on the metacommunity diversity of consumer species, and shows that hump-shaped relationships between local diversity and dispersal are not universal. Diversity-dispersal relationships can also be monotonically increasing or multimodal. Our work is a new step towards a general theory of metacommunity diversity integrating dispersal at multiple trophic levels.

Only Simpson diversity can be estimated accurately from microbial community fingerprints.

Lalande et al. (Microb. Ecol. 66(3):647-658, 2013) introduced a promising approach to quantify microbial diversity from fingerprinting profiles. Their analysis is based on extrapolating the abundance of the phylotypes detectable in a fingerprint towards the rare phylotypes of the community. By considering a set of reconstructed communities, Lalande et al. obtained a range of estimates for phylotype richness, Shannon diversity and Simpson diversity. They reported narrow ranges indicating accurate estimation, especially for Shannon and Simpson diversities. Here, we show that a much larger set of reconstructed communities than the one considered by Lalande et al. is consistent with the fingerprint. We find that the estimates for phylotype richness and Shannon diversity vary over orders of magnitude, but that the estimates for Simpson diversity are restricted to a narrow range (around 10 %). We conclude that only Simpson diversity can be estimated accurately from fingerprints.

Predicting coexistence of plants subject to a tolerance-competition trade-off.

Ecological trade-offs between species are often invoked to explain species coexistence in ecological communities. However, few mathematical models have been proposed for which coexistence conditions can be characterized explicitly in terms of a trade-off. Here we present a model of a plant community which allows such a characterization. In the model plant species compete for sites where each site has a fixed stress condition. Species differ both in stress tolerance and competitive ability. Stress tolerance is quantified as the fraction of sites with stress conditions low enough to allow establishment. Competitive ability is quantified as the propensity to win the competition for empty sites. We derive the deterministic, discrete-time dynamical system for the species abundances. We prove the conditions under which plant species can coexist in a stable equilibrium. We show that the coexistence conditions can be characterized graphically, clearly illustrating the trade-off between stress tolerance and competitive ability. We compare our model with a recently proposed, continuous-time dynamical system for a tolerance-fecundity trade-off in plant communities, and we show that this model is a special case of the continuous-time version of our model.

The abundance of snail hosts mediates the effects of antagonist interactions between trematodes on the transmission of human schistosomes.

BACKGROUND: Combating infectious diseases and halting biodiversity loss are intertwined challenges crucial to ensure global health. Biodiversity can constrain the spread of vector-borne pathogens circulation, necessitating a deeper understanding of ecological mechanisms underlying this pattern. Our study evaluates the relative importance of biodiversity and the abundance of Bulinus truncatus, a major intermediate host for the trematode Schistosoma haematobium on the circulation of this human pathogen at aquatic transmission sites. METHODS: We combined mathematical modelling and a molecular based empirical study to specifically assess the effect of co-infections between S. haematobium and other trematodes within their B. truncatus snail hosts; and B. truncatus abundance at transmission sites, on the production of S. haematobium infective cercariae stages released into the aquatic environment. RESULTS: Our modelling approach shows that more competitive trematode species exploiting B. truncatus as an intermediate host at the transmission site level leads to higher co-infection rates within snail hosts, subsequently reducing the production of S. haematobium cercariae. Conversely, an increase in B. truncatus abundance results in lower co-infection rates, and a higher proportion of S. haematobium cercariae released into the environment. Our empirical data from the field support these findings, indicating a significant negative effect of local trematode species richness (P-value = 0.029; AIC = 14.9) and co-infection rates (P-value = 0.02, AIC = 17.4) on the dominance of S. haematobium based on our GLMM models, while B. truncatus abundance positively influences S. haematobium dominance (P-value = 0.047, AIC = 20.1). CONCLUSIONS: Our study highlights the importance of biodiversity in influencing the transmission of S. haematobium through the effect of antagonistic interactions between trematodes within bulinid snail hosts. This effect intensifies when B. truncatus populations are low, promoting co-infections within snails. In line with the One Health concept, our results suggest that maintaining high level of freshwater biodiversity to sustain global trematode diversity at transmission sites can help reducing the circulation of Schistosoma species locally.

Predicting ecosystem stability from community composition and biodiversity.

As biodiversity is declining at an unprecedented rate, an important current scientific challenge is to understand and predict the consequences of biodiversity loss. Here, we develop a theory that predicts the temporal variability of community biomass from the properties of individual component species in monoculture. Our theory shows that biodiversity stabilises ecosystems through three main mechanisms: (1) asynchrony in species' responses to environmental fluctuations, (2) reduced demographic stochasticity due to overyielding in species mixtures and (3) reduced observation error (including spatial and sampling variability). Parameterised with empirical data from four long-term grassland biodiversity experiments, our prediction explained 22-75% of the observed variability, and captured much of the effect of species richness. Richness stabilised communities mainly by increasing community biomass and reducing the strength of demographic stochasticity. Our approach calls for a re-evaluation of the mechanisms explaining the effects of biodiversity on ecosystem stability.