Adaptive foraging of pollinators fosters gradual tipping under resource competition and rapid environmental change.

Plant and pollinator communities are vital for transnational food chains. Like many natural systems, they are affected by global change: rapidly deteriorating conditions threaten their numbers. Previous theoretical studies identified the potential for community-wide collapse above critical levels of environmental stressors-so-called bifurcation-induced tipping points. Fortunately, even as conditions deteriorate, individuals have some adaptive capacity, potentially increasing the boundary for a safe operating space where changes in ecological processes are reversible. Our study considers this adaptive capacity of pollinators to resource availability and identifies a new threat to disturbed pollinator communities. We model the adaptive foraging of pollinators in changing environments. Pollinator's adaptive foraging alters the dynamical responses of species, to the advantage of some-typically generalists-and the disadvantage of others, with systematic non-linear and non-monotonic effects on the abundance of particular species. We show that, in addition to the extent of environmental stress, the pace of change of environmental stress can also lead to the early collapse of both adaptive and nonadaptive pollinator communities. Specifically, perturbed communities exhibit rate-induced tipping points at stress levels within the safe boundary defined for constant stressors. With adaptive foraging, tipping is a more asynchronous collapse of species compared to nonadaptive pollinator communities, meaning that not all pollinator species reach a tipping event simultaneously. These results suggest that it is essential to consider the adaptive capacity of pollinator communities for monitoring and conservation. Both the extent and the rate of stress change relative to the ability of communities to recover are critical environmental boundaries.

Intermittent migration can induce pulses of speciation in a two-island system.

Geographic barriers can come and go depending on natural conditions. These fluctuations cause population cycles of expansion and contraction, introducing intermittent migrations that may not hinder speciation but rather promote diversification. Here, we study a neutral 2-island speciation model with intermittent migration driven by sea-level fluctuations. Seabed depth modulates isolation and connection periods between the islands, with migration occurring during connection periods with a certain probability. Mating is restricted to genetically compatible individuals on the same island and offspring inherit genomes from both parents through recombination. We observe speciation pulses that would not occur under strict isolation or continuous migration, with infrequent, temporary increases in species richness happening at different times depending on the combination of geographic settings and migration probability. The resulting dynamic patterns of richness exhibit contrasting behavior between connected and isolated scenarios, often including species that do not persist. Prolonged isolation can reduce richness to 1 species per island, resembling patterns commonly associated with archipelagos under sea-level fluctuations. Together with other studies, our results in out-of-equilibrium populations support the relevance of investigating the impact of variable migration on diversification, particularly in regions of high diversity.

Effect of Host-Switching on the Ecological and Evolutionary Patterns of Parasites.

Speciation via host-switching is a macroevolutionary process that emerges from a microevolutionary dynamic where individual parasites switch hosts, establish a new association, and reduce reproductive contact with the original parasite lineage. Phylogenetic distance and geographic distribution of the hosts have been shown to be determinants of the capacity and opportunity of the parasite to change hosts. Although speciation via host-switching has been reported in many host-parasite systems, its dynamic on the individual, population and community levels is poorly understood. Here we propose a theoretical model to simulate parasite evolution considering host-switching events on the microevolutionary scale, taking into account the macroevolutionary history of the hosts, to evaluate how host-switching can affect ecological and evolutionary patterns of parasites in empirical communities at regional and local scales. In the model, parasite individuals can switch hosts under variable intensity and have their evolution driven by mutation and genetic drift. Mating is sexual and only individuals that are sufficiently similar can produce offspring. We assumed that parasite evolution occurs at the same evolutionary time scale as their hosts, and that the intensity of host-switching decreases as the host species differentiate. Ecological and evolutionary patterns were characterized by the turnover of parasite species among host species, and parasite evolutionary tree imbalance respectively. We found a range of host-switching intensity that reproduces ecological and evolutionary patterns observed in empirical communities. Our results showed that turnover decreased as host-switching intensity increased, with low variation among the model replications. On the other hand, tree imbalance showed wide variation and non-monotonic tendency. We concluded that tree imbalance was sensitive to stochastic events, whereas turnover may be a good indicator of host-switching. We found that local communities corresponded to higher host-switching intensity when compared to regional communities, highlighting that spatial scale is a limitation for host-switching. [Dispersal of parasites, opportunity and capacity of interaction, phylogenetic conservatism, and community structure.].

Diversity patterns and speciation processes in a two-island system with continuous migration.

Geographic isolation is a central mechanism of speciation, but perfect isolation of populations is rare. Although speciation can be hindered if gene flow is large, intermediate levels of migration can enhance speciation by introducing genetic novelty in the semi-isolated populations or founding small communities of migrants. Here, we consider a two-island neutral model of speciation with continuous migration and study diversity patterns as a function of the migration probability, population size, and number of genes involved in reproductive isolation (dubbed as genome size). For small genomes, low levels of migration induce speciation on the islands that otherwise would not occur. Diversity, however, drops sharply to a single species inhabiting both islands as the migration probability increases. For large genomes, sympatric speciation occurs even when the islands are strictly isolated. Then species richness per island increases with the probability of migration, but the total number of species decreases as they become cosmopolitan. For each genome size, there is an optimal migration intensity for each population size that maximizes the number of species. We discuss the observed modes of speciation induced by migration and how they increase species richness in the insular system while promoting asymmetry between the islands and hindering endemism.

Interaction generalisation and demographic feedbacks drive the resilience of plant-insect networks to extinctions.

Understanding the processes driving ecological resilience, that is the extent to which systems retain their structure while absorbing perturbations, is a central challenge for theoretical and applied ecologists. Plant-insect assemblages are well-suited for the study of ecological resilience as they are species-rich and encompass a variety of ecological interactions that correspond to essential ecosystem functions. Mechanisms affecting community response to perturbations depend on both the natural history and structure of ecological interactions. Natural history attributes of the interspecific interactions, for example whether they are mutualistic or antagonistic, may affect the ecological resilience by controlling the demographic feedbacks driving ecological dynamics at the community level. Interaction generalisation may also affect resilience, by defining opportunities for interaction rewiring, the extent to which species are able to switch interactions in fluctuating environments. These natural history attributes may also interact with network structure to affect ecological resilience. Using adaptive network models, we investigated the resilience of plant-pollinator and plant-herbivore networks to species loss. We specifically investigated how fundamental natural history differences between these systems, namely the demographic consequences of the interaction and their level of generalisation-mediating rewiring opportunities-affect the resilience of dynamic ecological networks to extinctions. We also create a general benchmark for the effect of network structure on resilience simulating extinctions on theoretical networks with controlled structures. When network structure was static, pollination networks were less resilient than herbivory networks; this is related to their high levels of nestedness and the reciprocally positive feedbacks that define mutualisms, which made co-extinction cascades more likely and longer in plant-pollinator assemblages. When considering interaction rewiring, the high generalisation and the structure of pollination networks boosted their resilience to extinctions, which approached those of herbivory networks. Simulation results using theoretical networks suggested that the empirical structure of herbivory networks may protect them from collapse. Elucidating the ecological and evolutionary processes driving interaction rewiring is key to understanding the resilience of plant-insect assemblages. Accounting for rewiring requires ecologists to combine natural history with network models that incorporate feedbacks between species abundances, traits and interactions. This combination will elucidate how perturbations propagate at community level, reshaping biodiversity structure and ecosystem functions.

Compreender os processos que governam a resiliência dos sistemas ecológicos, i.e. o quanto sistemas ecológicos conservam sua estrutura enquanto absorvem perturbações, é um desafio central para ecólogos teóricos e aplicados. Comunidades de insetos e plantas são bons modelos para o estudo da resiliência ecológica pois são ricos em espécies, representando uma grande diversidade de interações ecológicas que correspondem a serviços ecossistêmicos essenciais. Os mecanismos que afetam a resposta de comunidades ecológicas a perturbações dependem tanto da história natural quanto da estrutura das interações ecológicas. A história natural de interações interespecíficas, e.g. se a interação é mutualística ou antagonística, pode afetar a resiliência do sistema ao controlar as retroalimentações demográficas que governam a dinâmica ecológica no nível da comunidade. Generalismo nas interações também pode afetar resiliência ao definir as oportunidades de rewiring de interações, i.e. o quanto espécies são capazes de mudar interações em ambientes instáveis. Atributos da história natural das interações podem também interagir com a estrutura de redes ecológicas de forma a influenciar a resiliência de sistemas ecológicos. Usando modelos de redes adaptativas, investigamos a resiliência de redes polinizador-planta e herbívoro-planta à perda de espécies. Especificamente, investigamos como diferenças fundamentais na história natural dos dois sistemas, isto é, as consequências demográficas da interação e seu grau de generalização - que mediam as oportunidades de rewiring - afetam a resiliência de redes ecológicas dinâmicas a extinções. Também criamos um referencial teórico e abrangente para o efeito da estrutura das redes em sua resiliência, simulando extinções em redes teóricas com estruturas controladas. Quando a estrutura das redes foi considerada estática, redes de polinização foram menos resilientes do que redes de herbivoria; o que está associado aos maiores níveis de aninhamento e aos efeitos demográficos positivos e recíprocos que definem mutualismos, aumentando a probabilidade e o comprimento das cascatas de extinção em redes polinizador-planta. Ao incorporar rewiring de interações, a alta generalização e a estrutura das redes de polinização impulsionou sua resiliência a extinções, que se aproximou da resiliência de redes de herbivoria. Os resultados das simulações com redes teóricas sugerem que estrutura de redes de herbivoria protegem esses sistemas do colapso. Compreender quais processos ecológicos e evolutivos governam o rewiring de interações é chave se queremos prever a resiliência de sistemas inseto-planta. Para incorporar rewiring de interações, será necessário combinar conhecimento sobre história natural com modelos de rede que incorporem a retroalimentação entre abundâncias, atributos e interações das espécies envolvidas. Essa combinação elucidará como perturbações se propagam no nível de comunidades ecológicas, reconfigurando a estrutura da biodiversidade e suas funções ecossistêmicas.

Signatures of Microevolutionary Processes in Phylogenetic Patterns.

Phylogenetic trees are representations of evolutionary relationships among species and contain signatures of the processes responsible for the speciation events they display. Inferring processes from tree properties, however, is challenging. To address this problem, we analyzed a spatially-explicit model of speciation where genome size and mating range can be controlled. We simulated parapatric and sympatric (narrow and wide mating range, respectively) radiations and constructed their phylogenetic trees, computing structural properties such as tree balance and speed of diversification. We showed that parapatric and sympatric speciation are well separated by these structural tree properties. Balanced trees with constant rates of diversification only originate in sympatry and genome size affected both the balance and the speed of diversification of the simulated trees. Comparison with empirical data showed that most of the evolutionary radiations considered to have developed in parapatry or sympatry are in good agreement with model predictions. Even though additional forces other than spatial restriction of gene flow, genome size, and genetic incompatibilities, do play a role in the evolution of species formation, the microevolutionary processes modeled here capture signatures of the diversification pattern of evolutionary radiations, regarding the symmetry and speed of diversification of lineages.

A genetic approach to the rock-paper-scissors game.

Polymorphisms are usually associated with defenses and mating strategies, affecting the individual's fitness. Coexistence of different morphs is, therefore, not expected, since the fittest morph should outcompete the others. Nevertheless, coexistence is observed in many natural systems. For instance, males of the side-blotched lizards (Uta stansburiana) present three morphs with throat colors orange, yellow and blue, which are associated with mating strategies and territorial behavior. The three male morphs compete for females in a system that is well described by the rock-paper-scissors dynamics of game theory. Previous studies have modeled the lizards as hermaphroditic populations whose individual's behavior were determined only by their phenotypes. Here we consider an extension of this dynamical system where diploidy and sexual reproduction are explicitly taken into account. Similarly to the lizards we represent the genetic system by a single locus with three alleles, o, y, and b in a diploid chromosome with dominance of o over y and of y over b. We show that this genotypic description of the dynamics results in the same equilibrium phenotype frequencies as the phenotypic models, but affects the stability of the system, changing the parameter region where coexistence of the three morphs is possible in a rock-paper-scissors game.

Nestedness across biological scales.

Biological networks pervade nature. They describe systems throughout all levels of biological organization, from molecules regulating metabolism to species interactions that shape ecosystem dynamics. The network thinking revealed recurrent organizational patterns in complex biological systems, such as the formation of semi-independent groups of connected elements (modularity) and non-random distributions of interactions among elements. Other structural patterns, such as nestedness, have been primarily assessed in ecological networks formed by two non-overlapping sets of elements; information on its occurrence on other levels of organization is lacking. Nestedness occurs when interactions of less connected elements form proper subsets of the interactions of more connected elements. Only recently these properties began to be appreciated in one-mode networks (where all elements can interact) which describe a much wider variety of biological phenomena. Here, we compute nestedness in a diverse collection of one-mode networked systems from six different levels of biological organization depicting gene and protein interactions, complex phenotypes, animal societies, metapopulations, food webs and vertebrate metacommunities. Our findings suggest that nestedness emerge independently of interaction type or biological scale and reveal that disparate systems can share nested organization features characterized by inclusive subsets of interacting elements with decreasing connectedness. We primarily explore the implications of a nested structure for each of these studied systems, then theorize on how nested networks are assembled. We hypothesize that nestedness emerges across scales due to processes that, although system-dependent, may share a general compromise between two features: specificity (the number of interactions the elements of the system can have) and affinity (how these elements can be connected to each other). Our findings suggesting occurrence of nestedness throughout biological scales can stimulate the debate on how pervasive nestedness may be in nature, while the theoretical emergent principles can aid further research on commonalities of biological networks.

The structure of ant-plant ecological networks: is abundance enough?

Knowledge of the mechanisms that shape biodiversity is essential to understand the ecological and evolutionary dynamics of interacting species. Recent studies posit that most of the organization of mutualistic networks is shaped by differences in species abundance among interacting species. In this study, we examined the mutualism involving plants with extrafloral nectaries and their associated ants. We show empirically that the difference in abundance among ants on vegetation partially explains the network structure of mutualistic interactions and that it is independent of ant species compositions: an ant species that is abundant usually interacts with more plant species. Moreover, nested networks are generated by simple variation in ant abundance on foliage. However, in ant-plant mutualistic networks, nestedness was higher than in networks describing the occurrence of ants on plants without a food resource. Additionally, the plant and ant species with the highest number of interactions within these networks interacted more among themselves than expected under the assumption of an abundance-based, random mixing of individuals. We hypothesize that the dominance of these ant species occurs because these ants are able to outcompete other ant species when feeding on extrafloral nectaries and because of the presence of ecophysiological adaptations to utilize liquid food.

Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms.

Mutualistic interactions involving pollination and ant-plant mutualistic networks typically feature tightly linked species grouped in modules. However, such modularity is infrequent in seed dispersal networks, presumably because research on those networks predominantly includes a single taxonomic animal group (e.g. birds). Herein, for the first time, we examine the pattern of interaction in a network that includes multiple taxonomic groups of seed dispersers, and the mechanisms underlying modularity. We found that the network was nested and modular, with five distinguishable modules. Our examination of the mechanisms underlying such modularity showed that plant and animal trait values were associated with specific modules but phylogenetic effect was limited. Thus, the pattern of interaction in this network is only partially explained by shared evolutionary history. We conclude that the observed modularity emerged by a combination of phylogenetic history and trait convergence of phylogenetically unrelated species, shaped by interactions with particular types of dispersal agents.