The signature of competition in ecomorphological traits across the avian radiation

Competition for shared resources represents a fundamental driver of biological diversity. However, the tempo and mode of phenotypic evolution in deep-time has been predominantly investigated using trait evolutionary models which assume that lineages evolve independently from each other. Consequently, the role of species interactions in driving macroevolutionary dynamics remains poorly understood. Here, we quantify the prevalence for signatures of competition between related species in the evolution of ecomorphological traits across the bird radiation. We find that mechanistic trait models accounting for the effect of species interactions on phenotypic divergence provide the best fit for the data on at least one trait axis in 27 out of 59 clades ranging between 21 and 195 species. Where it occurs, the signature of competition generally coincides with positive species diversity-dependence, driven by the accumulation of lineages with similar ecologies, and we find scarce evidence for trait-dependent or negative diversity-dependent phenotypic evolution. Overall, our results suggest that the footprint of interspecific competition is often eroded in long-term patterns of phenotypic diversification, and that other selection pressures may predominantly shape ecomorphological diversity among extant species at macroevolutionary scales.     

Opportunistic attachment assembles plant–pollinator networks

Species and interactions are being lost at alarming rates and it is imperative to understand how communities assemble if we have to prevent their collapse and restore lost interactions. Using an 8‐year dataset comprising nearly 20 000 pollinator visitation records, we explore the assembly of plant–pollinator communities at native plant restoration sites in an agricultural landscape. We find that species occupy highly dynamic network positions through time, causing the assembly process to be punctuated by major network reorganisations. The most persistent pollinator species are also the most variable in their network positions, contrary to what preferential attachment – the most widely studied theory of ecological network assembly – predicts. Instead, we suggest assembly occurs via an opportunistic attachment process. Our results contribute to our understanding of how communities assembly and how species interactions change through time while helping to inform efforts to reassemble robust communities.     

Ecological integration of alien species into a tree-parasitic fungus network

The diversification of species and their interactions during the course of evolution has produced ecological networks with a complex topology. This topology influences the current functioning of ecosystems. It is therefore important to investigate whether the species introduced recently by human activities have merged seamlessly into recipient ecological networks by developing interactions quantitatively and qualitatively similar to those of native species, or whether their establishment has altered the topology of the networks. We tackled this issue in the case of a well resolved interaction network between 51 forest tree taxa and 154 pathogenic fungal species. We found that alien and native species with similar phylogenetic histories and life-history strategies had similar types and numbers of interactions. Our results also suggest that the clustered architecture of the network has not been altered by the integration of alien species. It therefore seems that a few centuries have been sufficient for the network to assimilate the newly introduced species. This rapid integration was unexpected for a plant-pathogen network, because selection acts continually on plants, favouring the emergence of defences against new pathogens and impeding the development of new interactions. However, it was recently shown that perturbation of the structure of ecological networks might be overlooked if species interactions are not quantified. The tree-parasitic fungus network considered in this study is binary. We might therefore end up with different results by using quantitative data.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

Comparative interactomics analysis of protein family interaction networks using PSIMAP (protein structural interactome map)

MOTIVATION: Many genomes have been completely sequenced. However, detecting and analyzing their protein-protein interactions by experimental methods such as co-immunoprecipitation, tandem affinity purification and Y2H is not as fast as genome sequencing. Therefore, a computational prediction method based on the known protein structural interactions will be useful to analyze large-scale protein-protein interaction rules within and among complete genomes. RESULTS: We confirmed that all the predicted protein family interactomes (the full set of protein family interactions within a proteome) of 146 species are scale-free networks, and they share a small core network comprising 36 protein families related to indispensable cellular functions. We found two fundamental differences among prokaryotic and eukaryotic interactomes: (1) eukarya had significantly more hub families than archaea and bacteria and (2) certain special hub families determined the topology of the eukaryotic interactomes. Our comparative analysis suggests that a very small number of expansive protein families led to the evolution of interactomes and seemed to have played a key role in species diversification. SUPPLEMENTARY INFORMATION: http://interactomics.org.     

The robustness of the Webworld model to changes in its structure

We investigate the robustness of a co-evolutionary model of multi-species communities to changes in its structure. The model has both a conventional population dynamics and a network dynamics through which new species are introduced and unsuccessful species removed. The effect of choosing different forms of population dynamics has already been investigated for this model. Here we study the effects of changing the nature of species interactions and thresholds such as the number of individuals of a species required to be present before that species is said to be extinct. We find that the model is remarkably robust to these changes, with only a very few of the modifications leading to food webs which differ appreciably from those found in the original model. This indicates that many aspects of the structure of the model are not, in general, a factor in determining the nature of the food webs constructed.     

Detecting local diversity‐dependence in diversification

Whether there are ecological limits to species diversification is a hotly debated topic. Molecular phylogenies show slowdowns in lineage accumulation, suggesting that speciation rates decline with increasing diversity. A maximum‐likelihood (ML) method to detect diversity‐dependent (DD) diversification from phylogenetic branching times exists, but it assumes that diversity‐dependence is a global phenomenon and therefore ignores that the underlying species interactions are mostly local, and not all species in the phylogeny co‐occur locally. Here, we explore whether this ML method based on the nonspatial diversity‐dependence model can detect local diversity‐dependence, by applying it to phylogenies, simulated with a spatial stochastic model of local DD speciation, extinction, and dispersal between two local communities. We find that type I errors (falsely detecting diversity‐dependence) are low, and the power to detect diversity‐dependence is high when dispersal rates are not too low. Interestingly, when dispersal is high the power to detect diversity‐dependence is even higher than in the nonspatial model. Moreover, estimates of intrinsic speciation rate, extinction rate, and ecological limit strongly depend on dispersal rate. We conclude that the nonspatial DD approach can be used to detect diversity‐dependence in clades of species that live in not too disconnected areas, but parameter estimates must be interpreted cautiously.     

Phylogenetic origins of local-scale diversity patterns and the causes of Amazonian megadiversity

What explains the striking variation in local species richness across the globe and the remarkable diversity of rainforest sites in Amazonia? Here, we apply a novel phylogenetic approach to these questions, using treefrogs (Hylidae) as a model system. Hylids show dramatic variation in local richness globally and incredible local diversity in Amazonia. We find that variation in local richness is not explained primarily by climatic factors, rates of diversification (speciation and extinction) nor morphological variation. Instead, local richness patterns are explained predominantly by the timing of colonization of each region, and Amazonian megadiversity is linked to the long-term sympatry of multiple clades in that region. Our results also suggest intriguing interactions between clade diversification, trait evolution and the accumulation of local richness. Specifically, sympatry between clades seems to slow diversification and trait evolution, but prevents neither the accumulation of local richness over time nor the co-occurrence of similar species.     

Did pollination shifts drive diversification in southern African Gladiolus? Evaluating the model of pollinator-driven speciation

The pollinator-driven ecological speciation model has frequently been invoked to explain plant richness in biodiversity hotspots. Here, by focusing on Gladiolus (260 species), a flagship example of a clade with diverse pollination biology, we test the hypothesis that high species diversity in southern Africa, one of the world's most floristically rich regions, has primarily been driven by ecological shifts in pollination systems. We use phylogenetic methods to estimate rates of transition between the seven highly specialized pollination strategies in Gladiolus. We find that pollination systems have evolved multiple times and that some pollination strategies arose by a variety of evolutionary pathways. Pollination shifts account for up to one-third of all lineage splitting events in the genus, providing partial support for the pollinator-driven speciation model. Transitions from the ancestral pollination mode to derived systems have also resulted in increased rates of diversification, suggesting that certain pollination systems may speed up speciation processes, independently of pollination shifts per se. This study suggests that frequent pollination shifts have played a role in driving high phenotypic and species diversity but indicates that additional factors need to be invoked to account for the spectacular diversification in southern African Gladiolus.     

Simulated evolution of protein-protein interaction networks with realistic topology

We model the evolution of eukaryotic protein-protein interaction (PPI) networks. In our model, PPI networks evolve by two known biological mechanisms: (1) Gene duplication, which is followed by rapid diversification of duplicate interactions. (2) Neofunctionalization, in which a mutation leads to a new interaction with some other protein. Since many interactions are due to simple surface compatibility, we hypothesize there is an increased likelihood of interacting with other proteins in the target protein's neighborhood. We find good agreement of the model on 10 different network properties compared to high-confidence experimental PPI networks in yeast, fruit flies, and humans. Key findings are: (1) PPI networks evolve modular structures, with no need to invoke particular selection pressures. (2) Proteins in cells have on average about 6 degrees of separation, similar to some social networks, such as human-communication and actor networks. (3) Unlike social networks, which have a shrinking diameter (degree of maximum separation) over time, PPI networks are predicted to grow in diameter. (4) The model indicates that evolutionarily old proteins should have higher connectivities and be more centrally embedded in their networks. This suggests a way in which present-day proteomics data could provide insights into biological evolution.     

Density-dependent diversification in North American wood warblers

Evidence from both molecular phylogenies and the fossil record suggests that rates of species diversification often decline through time during evolutionary radiations. One proposed explanation for this pattern is ecological opportunity, whereby an initial abundance of resources and lack of potential competitors facilitate rapid diversification. This model predicts density-dependent declines in diversification rates, but has not been formally tested in any species-level radiation. Here we develop a new conceptual framework that distinguishes density dependence from alternative processes that also produce temporally declining diversification, and we demonstrate this approach using a new phylogeny of North American Dendroica wood warblers. We show that explosive lineage accumulation early in the history of this avian radiation is best explained by a density-dependent diversification process. Our results suggest that the tempo of wood warbler diversification was mediated by ecological interactions among species and that lineage and ecological diversification in this group are coupled, as predicted under the ecological opportunity model.     

Dynamics and Structure in Cell Signaling Networks: Off-State Stability and Dynamically Positive Cycles

The signaling system is a fundamental part of the cell, as it regulates essential functions including growth, differentiation, protein synthesis, and apoptosis. A malfunction in this subsystem can disrupt the cell significantly, and is believed to be involved in certain diseases, with cancer being a very important example. While the information available about intracellular signaling networks is constantly growing, and the network topology is actively being analyzed, the modeling of the dynamics of such a system faces difficulties due to the vast number of parameters, which can prove hard to estimate correctly. As the functioning of the signaling system depends on the parameters in a complex way, being able to make general statements based solely on the network topology could be especially appealing. We study a general kinetic model of the signaling system, giving results for the asymptotic behavior of the system in the case of a network with only activatory interactions. We also investigate the possible generalization of our results for the case of a more general model including inhibitory interactions too. We find that feedback cycles made up entirely of activatory interactions (which we call dynamically positive) are especially important, as their properties determine whether the system has a stable signal-off state, which is desirable in many situations to avoid autoactivation due to a noisy environment. To test our results, we investigate the network topology in the Signalink database, and find that the human signaling network indeed has only significantly few dynamically positive cycles, which agrees well with our theoretical arguments.     

Intestinal microflora and diversification of the rabbit antibody repertoire

The rabbit establishes its primary Ab repertoire by somatically diversifying an initial repertoire that is limited by restricted VH gene segment usage during VDJ gene rearrangement. Somatic diversification occurs in gut-associated lymphoid tissue (GALT), and by about 1-2 mo of age nearly all Ig VDJ genes are somatically diversified. In other species that are known to establish their primary Ab repertoire by somatic diversification, such as chicken, sheep, and cattle, diversification appears to be developmentally regulated: it begins before birth and occurs independent of exogenous factors. Because somatic diversification in rabbit occurs well after birth in GALT, the diversification process may not be developmentally regulated, but may require interaction with exogenous factors derived from the gut. To test this hypothesis, we examined Ab repertoire diversification in rabbits in which the appendix was ligated shortly after birth to prevent microbial colonization and all other organized GALT was surgically removed. We found that by 12 wk of age nearly 90% of the Ig VDJ genes in PBL were undiversified, indicating that intestinal microflora are required for somatically diversifying the Ab repertoire. We also examined repertoire diversification in sterilely derived remote colony rabbits that were hand raised away from contact with conventional rabbits and thereby acquired a different gut microflora. In these remote colony rabbits, GALT was underdeveloped, and 70% of the Ig VDJ genes in PBL were undiversified. We conclude that specific, currently unidentified intestinal microflora are required for Ab repertoire diversification.     

Diversity in a complex ecological network with two interaction types

Most studies on ecological networks consider only a single interaction type (e.g. competitive, predatory or mutualistic), and try to developrules for system stability based exclusively on properties of this interaction type. However, the stability of ecological networks may be more dependent on the way different interaction types are combined in real communities. To address this issue, we start by compiling an ecological network in the Doñana Biological Reserve, southern Spain, with 390 species and 798 mu-tualistic and antagonistic interactions. We characterize network structure by looking at how mutualistic and antagonistic interactions are combined across all plant species. Both the ratio of mutualistic to antagonistic interactions per plant, and the number of basic modules with an antagonistic and a mutualistic interaction are very heterogeneous across plant species, with a few plant species showing very high values for these parameters. To assess the implications of these network patterns on species diversity, we study analytically and by simulation a model of this ecological network. We find that the observed correlation between strong interaction strengths and high mutualistic to antagonistic ratios in a few plant species significantly increases community diversity. Thus, to predict the persistence of biodiversity we need to understand how interaction strength and the architecture of ecological networks with different interaction types are combined.     

Evaluating mechanisms of diversification in a Guineo‐Congolian tropical forest frog using demographic model selection

The accumulation of biodiversity in tropical forests can occur through multiple allopatric and parapatric models of diversification, including forest refugia, riverine barriers and ecological gradients. Considerable debate surrounds the major diversification process, particularly in the West African Lower Guinea forests, which contain a complex geographic arrangement of topographic features and historical refugia. We used genomic data to investigate alternative mechanisms of diversification in the Gaboon forest frog, Scotobleps gabonicus, by first identifying population structure and then performing demographic model selection and spatially explicit analyses. We found that a majority of population divergences are best explained by allopatric models consistent with the forest refugia hypothesis and involve divergence in isolation with subsequent expansion and gene flow. These population divergences occurred simultaneously and conform to predictions based on climatically stable regions inferred through ecological niche modelling. Although forest refugia played a prominent role in the intraspecific diversification of S. gabonicus, we also find evidence for potential interactions between landscape features and historical refugia, including major rivers and elevational barriers such as the Cameroonian Volcanic Line. We outline the advantages of using genomewide variation in a model‐testing framework to distinguish between alternative allopatric hypotheses, and the pitfalls of limited geographic and molecular sampling. Although phylogeographic patterns are often species‐specific and related to life‐history traits, additional comparative studies incorporating genomic data are necessary for separating shared historical processes from idiosyncratic responses to environmental, climatic and geological influences on diversification.     

Mutualistic mimicry enhances species diversification through spatial segregation and extension of the ecological niche space

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large‐scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population‐based model. We focus on mutualistic Müllerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Müllerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Müllerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Müllerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Müllerian mimicry on ecological, spatial, and phylogenetic diversification.     

Biological factors contributing to bark and ambrosia beetle species diversification

The study of species diversification can identify the processes that shape patterns of species richness across the tree of life. Here, we perform comparative analyses of species diversification using a large dataset of bark beetles. Three examined covariates—permanent inbreeding (sibling mating), fungus farming, and major host type—represent a range of factors that may be important for speciation. We studied the association of these covariates with species diversification while controlling for evolutionary lag on adaptation. All three covariates were significantly associated with diversification, but fungus farming showed conflicting patterns between different analyses. Genera that exhibited interspecific variation in host type had higher rates of species diversification, which may suggest that host switching is a driver of species diversification or that certain host types or forest compositions facilitate colonization and thus allopatric speciation. Because permanent inbreeding is thought to facilitate dispersal, the positive association between permanent inbreeding and diversification rates suggests that dispersal ability may contribute to species richness. Bark beetles are ecologically unique; however, our results indicate that their impressive species diversity is largely driven by mechanisms shown to be important for many organism groups.     

Local and collective transitions in sparsely-interacting ecological communities

Interactions in natural communities can be highly heterogeneous, with any given species interacting appreciably with only some of the others, a situation commonly represented by sparse interaction networks. We study the consequences of sparse competitive interactions, in a theoretical model of a community assembled from a species pool. We find that communities can be in a number of different regimes, depending on the interaction strength. When interactions are strong, the network of coexisting species breaks up into small subgraphs, while for weaker interactions these graphs are larger and more complex, eventually encompassing all species. This process is driven by the emergence of new allowed subgraphs as interaction strength decreases, leading to sharp changes in diversity and other community properties, and at weaker interactions to two distinct collective transitions: a percolation transition, and a transition between having a unique equilibrium and having multiple alternative equilibria. Understanding community structure is thus made up of two parts: first, finding which subgraphs are allowed at a given interaction strength, and secondly, a discrete problem of matching these structures over the entire community. In a shift from the focus of many previous theories, these different regimes can be traversed by modifying the interaction strength alone, without need for heterogeneity in either interaction strengths or the number of competitors per species.     

Are rates of species diversification correlated with rates of morphological evolution?

Some major evolutionary theories predict a relationship between rates of proliferation of new species (species diversification) and rates of morphological divergence between them. However, this relationship has not been rigorously tested using phylogeny-based approaches. Here, we test this relationship with morphological and phylogenetic data from 190 species of plethodontid salamanders. Surprisingly, we find that rates of species diversification and morphological evolution are not significantly correlated, such that rapid diversification can occur with little morphological change, and vice versa. We also find that most clades have undergone remarkably similar patterns of morphological evolution (despite extensive sympatry) and that those relatively novel phenotypes are not associated with rapid diversification. Finally, we find a strong relationship between rates of size and shape evolution, which has not been previously tested.     

Bringing Elton and Grinnell together: a quantitative framework to represent the biogeography of ecological interaction networks

Biogeography has traditionally focused on the spatial distribution and abundance of species. Both are driven by the way species interact with one another, but only recently community ecologists realized the need to document their spatial and temporal variation. Here, we call for an integrated approach, adopting the view that community structure is best represented as a network of ecological interactions, and show how it translates to biogeography questions. We propose that the ecological niche should encompass the effect of the environment on species distribution (the Grinnellian dimension of the niche) and on the ecological interactions among them (the Eltonian dimension). Starting from this concept, we develop a quantitative theory to explain turnover of interactions in space and time – i.e. a novel approach to interaction distribution modeling. We apply this framework to host–parasite interactions across Europe and find that two aspects of the environment (temperature and precipitation) exert a strong imprint on species co‐occurrence, but not on species interactions. Even where species co‐occur, interaction proves to be stochastic rather than deterministic, adding to variation in realized network structure. We also find that a large majority of host‐parasite pairs are never found together, thus precluding any inferences regarding their probability to interact. This first attempt to explain variation of network structure at large spatial scales opens new perspectives at the interface of species distribution modeling and community ecology.