Interspecific interactions affect species and community responses to climate shifts

The response of individual species to climate change may alter the composition and dynamics of communities. Here, we show that the impacts of environmental change on communities can depend on the nature of the interspecific interactions: mutualistic communities typically respond differently than commensalistic or parasitic communities. We model and analyse the geographic range shifting of metapopulations of two interacting species – a host and an obligate species. Different types of interspecific interactions are implemented by modifying local extinction rates according to the presence/absence of the other species. We distinguish and compare three fundamentally different community types: mutualism, commensalism and parasitism. We find that community dynamics during geographic range shifting critically depends on the type of interspecific interactions. Parasitic interactions exacerbate the negative effect of environmental change whereas mutualistic interactions only partly compensate it. Commensalistic interactions exhibit an intermediate response. Based on these model outcomes, we predict that parasitic species interactions may be more vulnerable to geographic range shifting than commensalistic or mutualistic ones. However, we observe that when climate stabilises following a period of change, the rate of community recovery is largely independent of the type of interspecific interactions. These results emphasize that communities respond delicately to environmental change, and that local interspecific interactions can affect range shifting communities at large spatial scales.     

Exploring the tempo of species diversification in legumes

Whatever criteria are used to measure evolutionary success – species numbers, geographic range, ecological abundance, ecological and life history diversity, background diversification rates, or the presence of rapidly evolving clades – the legume family is one of the most successful lineages of flowering plants. Despite this, we still know rather little about the dynamics of lineage and species diversification across the family through the Cenozoic, or about the underlying drivers of diversification. There have been few attempts to estimate net species diversification rates or underlying speciation and extinction rates for legume clades, to test whether among-lineage variation in diversification rates deviates from null expectations, or to locate species diversification rate shifts on specific branches of the legume phylogenetic tree. In this study, time-calibrated phylogenetic trees for a set of species-rich legume clades – Calliandra, Indigofereae, Lupinus, Mimosa and Robinieae – and for the legume family as a whole, are used to explore how we might approach these questions. These clades are analysed using recently developed maximum likelihood and Bayesian methods to detect species diversification rate shifts and test for among-lineage variation in speciation, extinction and net diversification rates. Possible explanations for rate shifts in terms of extrinsic factors and/or intrinsic trait evolution are discussed. In addition, several methodological issues and limitations associated with these analyses are highlighted emphasizing the potential to improve our understanding of the evolutionary dynamics of legume diversification by using much more densely sampled phylogenetic trees that integrate information across broad taxonomic, geographical and temporal levels.     

Mutualism with plants drives primate diversification

Understanding the origin of diversity is a fundamental problem in biology. Evolutionary diversification has been intensely explored during the last years due to the development of molecular tools and the comparative method. However, most studies are conducted using only information from extant species. This approach probably leads to misleading conclusions, especially because of inaccuracy in the estimation of extinction rates. It is critical to integrate the information generated by extant organisms with the information obtained from the fossil record. Unfortunately, this integrative approach has been seldom performed, and thus, our understanding of the factors fueling diversification is still deficient. Ecological interactions are a main factor shaping evolutionary diversification by influencing speciation and extinction rates. Most attention has focused on the effect of antagonistic interactions on evolutionary diversification. In contrast, the role of mutualistic interactions in shaping diversification has been much less explored. In this study, by combining phylogenetic, neontological, and paleontological information, we show that a facultative mutualistic plant-animal interaction emerging from frugivory and seed dispersal has most likely contributed to the diversification of our own lineage, the primates. We compiled diet and seed dispersal ability in 381 extant and 556 extinct primates. Using well-established molecular phylogenies, we demonstrated that mutualistic extant primates had higher speciation rates, lower extinction rates, and thereby higher diversification rates than nonmutualistic ones. Similarly, mutualistic fossil primates had higher geological durations and smaller per capita rates of extinction than nonmutualistic ones. As a mechanism underlying this pattern, we found that mutualistic extinct and extant primates have significantly larger geographic ranges, which promotes diversification by hampering extinction and increasing geographic speciation. All these outcomes together strongly suggest that the establishment of a facultative mutualism with plants has greatly benefited primate evolution and fueled its taxonomic diversification.     

Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human‐driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.     

SCALE AND HIERARCHY IN MACROEVOLUTION

Abstract: Scale and hierarchy must be incorporated into any conceptual framework for the study of macroevolution, i.e. evolution above the species level. Expansion of temporal and spatial scales reveals evolutionary patterns and processes that are virtually inaccessible to, and unpredictable from, short‐term, localized observations. These larger‐scale phenomena range from evolutionary stasis at the species level and the mosaic assembly of complex morphologies in ancestral forms to the non‐random distribution in time and space of the origin of major evolutionary novelties, as exemplified by the Cambrian explosion and post‐extinction recoveries of metazoans, and the preferential origin of major marine groups in onshore environments and tropical waters. Virtually all of these phenomena probably involve both ecological and developmental factors, but the integration of these components with macroevolutionary theory has only just begun. Differential survival and reproduction of units can occur at several levels within a biological hierarchy that includes DNA sequences, organisms, species and clades. Evolution by natural selection can occur at any level where there is heritable variation that affects birth and death of units by virtue of interaction with the environment. This dynamic can occur when selfish DNA sequences replicate disproportionately within genomes, when organisms enjoy fitness advantages within populations (classical Darwinian selection), when differential speciation or extinction occurs within clades owing to organismic properties (effect macroevolution), and when differential speciation or extinction occurs within clades owing to emergent, species‐level properties (in the strict sense species selection). Operationally, emergent species‐level properties such as geographical range can be recognized by testing whether their macroevolutionary effects are similar regardless of the different lower‐level factors that produce them. Large‐scale evolutionary trends can be driven by transformation of species, preferential production of species in a given direction, differential origination or extinction, or any combination of these; the potential for organismic traits to hitch‐hike on other factors that promote speciation or damp extinction is high. Additional key attributes of macroevolutionary dynamics within biological hierarchies are that (1) hierarchical levels are linked by upward and downward causation, so that emergent properties at a focal level do not impart complete independence; (2) hierarchical effects are asymmetrical, so that dynamics at a given focal level need not propagate upwards, but will always cascade downwards; and (3) rates are generally, although not always, faster at lower hierarchical levels. Temporal and spatial patterns in the origin of major novelties and higher taxa are significantly discordant from those at the species and genus levels, suggesting complex hierarchical effects that remain poorly understood. Not only are many of the features promoting survivorship during background times ineffective during mass extinctions, but also they are replaced in at least some cases by higher‐level, irreducible attributes such as clade‐level geographical range. The incorporation of processes that operate across hierarchical levels and a range of temporal and spatial scales has expanded and enriched our understanding of evolution.     

Biological hierarchies and the nature of extinction

Hierarchy theory recognises that ecological and evolutionary units occur in a nested and interconnected hierarchical system, with cascading effects occurring between hierarchical levels. Different biological disciplines have routinely come into conflict over the primacy of different forcing mechanisms behind evolutionary and ecological change. These disconnects arise partly from differences in perspective (with some researchers favouring ecological forcing mechanisms while others favour developmental/historical mechanisms), as well as differences in the temporal framework in which workers operate. In particular, long‐term palaeontological data often show that large‐scale (macro) patterns of evolution are predominantly dictated by shifts in the abiotic environment, while short‐term (micro) modern biological studies stress the importance of biotic interactions. We propose that thinking about ecological and evolutionary interactions in a hierarchical framework is a fruitful way to resolve these conflicts. Hierarchy theory suggests that changes occurring at lower hierarchical levels can have unexpected, complex effects at higher scales due to emergent interactions between simple systems. In this way, patterns occurring on short‐ and long‐term time scales are equally valid, as changes that are driven from lower levels will manifest in different forms at higher levels. We propose that the dual hierarchy framework fits well with our current understanding of evolutionary and ecological theory. Furthermore, we describe how this framework can be used to understand major extinction events better. Multi‐generational attritional loss of reproductive fitness (MALF) has recently been proposed as the primary mechanism behind extinction events, whereby extinction is explainable solely through processes that result in extirpation of populations through a shutdown of reproduction. While not necessarily explicit, the push to explain extinction through solely population‐level dynamics could be used to suggest that environmentally mediated patterns of extinction or slowed speciation across geological time are largely artefacts of poor preservation or a coarse temporal scale. We demonstrate how MALF fits into a hierarchical framework, showing that MALF can be a primary forcing mechanism at lower scales that still results in differential survivorship patterns at the species and clade level which vary depending upon the initial environmental forcing mechanism. Thus, even if MALF is the primary mechanism of extinction across all mass extinction events, the primary environmental cause of these events will still affect the system and result in differential responses. Therefore, patterns at both temporal scales are relevant.     

Understanding extinction debts: spatio–temporal scales,mechanisms and a roadmap for future research

Extinction debt refers to delayed species extinctions expected as a consequence of ecosystem perturbation. Quantifying such extinctions and investigating long‐term consequences of perturbations has proven challenging, because perturbations are not isolated and occur across various spatial and temporal scales, from local habitat losses to global warming. Additionally, the relative importance of eco‐evolutionary processes varies across scales, because levels of ecological organization, i.e. individuals, (meta)populations and (meta)communities, respond hierarchically to perturbations. To summarize our current knowledge of the scales and mechanisms influencing extinction debts, we reviewed recent empirical, theoretical and methodological studies addressing either the spatio–temporal scales of extinction debts or the eco‐evolutionary mechanisms delaying extinctions. Extinction debts were detected across a range of ecosystems and taxonomic groups, with estimates ranging from 9 to 90% of current species richness. The duration over which debts have been sustained varies from 5 to 570 yr, and projections of the total period required to settle a debt can extend to 1000 yr. Reported causes of delayed extinctions are 1) life‐history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Other potential factors that may extend survival time such as microevolutionary dynamics, or delayed extinctions of interaction partners, have rarely been analyzed. Therefore, we propose a roadmap for future research with three key avenues: 1) the microevolutionary dynamics of extinction processes, 2) the disjunctive loss of interacting species and 3) the impact of multiple regimes of perturbation on the payment of debts. For their ability to integrate processes occurring at different levels of ecological organization, we highlight mechanistic simulation models as tools to address these knowledge gaps and to deepen our understanding of extinction dynamics.     

A model of onshore-offshore change in faunal diversity

Onshore-offshore patterns of faunal change occurred at many taxonomic scales during the Paleozoic Era, ranging from replacement of the Cambrian evolutionary fauna by the Paleozoic fauna to the environmental expansion of many orders and classes. A simple mathematical model is constructed to investigate such change. The environmental gradient across the marine shelf-slope is treated as a linear array of discrete habitats, each of which holds a set number of species, as observed in the fossil record. During any interval of time, some portion of the species in each habitat becomes extinct by background processes, with rates of extinction varying among both clades and habitats, as also observed in the record. After extinction, species are replaced from within the habitat and from immediately adjacent habitats, with proportions dependent on surviving species. This model leads to the prediction that extinction-resistant clades will always diversify at the expense of extinction-prone clades. But if extinction intensity is highest in nearshore habitats, extinction-resistant clades will expand preferentially in the onshore direction, build up diversity there, and then diversify outward toward the offshore. Thus, onshore-offshore patterns of diversification may be the expectation for faunal change quite independently of whether or not clades originate onshore. When the model is parameterized for Paleozoic trilobites and brachiopods, numerical solutions exhibit both a pattern of faunal change and a time span for diversification similar to that seen in the fossil record. They also generate structure similar to that seen in global diversification, including logistic patterns of growth, declining origination but constant extinction within clades through time, and declining overall extinction across clades through time.     

The effect of ant association on the population genetics of the Australian butterfly Jalmenus evagoras (Lepidoptera: Lycaenidae)

Populations of the myrmecophilous lycaenid Jalmenus evagoras Donovan were assessed for genetic structure at three hierarchical spatial scales: sites, geographically-defined subpopulations, and subpopulations defined by species of mutualistic ant-associate. Estimates of Wright's FST generated from multilocus electrophoretic data revealed low, though significant, amounts of genetic structure. Most structure was observed at the level of geographic subpopulations, suggesting that adult butterflies do not exhibit preferential mating and oviposition along the lines of ant associate. The genetic structure data, together with estimates of Nei's genetic distance (D) for pairwise site and subpopulation comparisons, suggest that J. evagoras populations are spatially and temporally dynamic. These patterns are considered in the context of extinction and recolonization models. The extreme patchiness of J. evagoras populations stems from the stringent requirements of both host plant and host ant, contributing to an extinction/ recolonization process. We discuss the key parameters influencing genetic cohesion versus differentiation under an extinction/recolonization regime, including mode of butterfly dispersal, site turnover rate, and the effects of host dispersal and phenology. This system provides a model of population-level consequences of certain mutualistic interactions as well as of a class of patterns arising from an extinction/recolonization process.     

Mutualistic interactions shape global spatial congruence and climatic niche evolution in Neotropical mimetic butterflies

Understanding the mechanisms underlying species distributions and coexistence is both a priority and a challenge for biodiversity hotspots such as the Neotropics. Here, we highlight that Müllerian mimicry, where defended prey species display similar warning signals, is key to the maintenance of biodiversity in the c. 400 species of the Neotropical butterfly tribe Ithomiini (Nymphalidae: Danainae). We show that mimicry drives large-scale spatial association among phenotypically similar species, providing new empirical evidence for the validity of Müller's model at a macroecological scale. Additionally, we show that mimetic interactions drive the evolutionary convergence of species climatic niche, thereby strengthening the co-occurrence of co-mimetic species. This study provides new insights into the importance of mutualistic interactions in shaping both niche evolution and species assemblages at large spatial scales. Critically, in the context of climate change, our results highlight the vulnerability to extinction cascades of such adaptively assembled communities tied by positive interactions.     

Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity

Many groups show higher species richness in tropical regions but the underlying causes remain unclear. Despite many competing hypotheses to explain latitudinal diversity gradients, only three processes can directly change species richness across regions: speciation, extinction and dispersal. These processes can be addressed most powerfully using large-scale phylogenetic approaches, but most previous studies have focused on small groups and recent time scales, or did not separate speciation and extinction rates. We investigate the origins of high tropical diversity in amphibians, applying new phylogenetic comparative methods to a tree of 2871 species. Our results show that high tropical diversity is explained by higher speciation in the tropics, higher extinction in temperate regions and limited dispersal out of the tropics compared with colonization of the tropics from temperate regions. These patterns are strongly associated with climate-related variables such as temperature, precipitation and ecosystem energy. Results from models of diversity dependence in speciation rate suggest that temperate clades may have lower carrying capacities and may be more saturated (closer to carrying capacity) than tropical clades. Furthermore, we estimate strikingly low tropical extinction rates over geological time scales, in stark contrast to the dramatic losses of diversity occurring in tropical regions presently.     

Themes from variation: probing the commonalities of symbiotic associations

Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium "Living Together: the Dynamics of Symbiotic Interactions" considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbiotic associations? 6. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations?Two themes emerged from the symposium. First, all the participants have incorporated multiple techniques and perspectives into their work, approaches which facilitate the understanding of symbiotic dynamics at several levels of biological organization. Secondly, many of the papers addressed genetic and environmental variation in symbiotic interactions. Such approaches are useful tools for analysis of the mechanics of interspecies interactions and for characterization of the most important factors which influence them. They provide us with the tools to evaluate symbioses in a world of complexity, variation and change.     

Evolutionary conservatism and convergence both lead to striking similarity in ecology,morphology and performance across continents in frogs

Many clades contain ecologically and phenotypically similar species across continents, yet the processes generating this similarity are largely unstudied, leaving fundamental questions unanswered. Is similarity in morphology and performance across assemblages caused by evolutionary convergence or by biogeographic dispersal of evolutionarily conserved ecotypes? Does convergence to new ecological conditions erase evidence of past adaptation? Here, we analyse ecology, morphology and performance in frog assemblages from three continents (Asia, Australia and South America), assessing the importance of dispersal and convergent evolution in explaining similarity across regions. We find three striking results. First, species using the same microhabitat type are highly similar in morphology and performance across both clades and continents. Second, some species on different continents owe their similarity to dispersal and evolutionary conservatism (rather than evolutionary convergence), even over vast temporal and spatial scales. Third, in one case, an ecologically specialized ancestor radiated into diverse ecotypes that have converged with those on other continents, largely erasing traces of past adaptation to their ancestral ecology. Overall, our study highlights the roles of both evolutionary conservatism and convergence in explaining similarity in species traits over large spatial and temporal scales and demonstrates a statistical framework for addressing these questions in other systems.     

Pattern of functional extinctions in ecological networks with a variety of interaction types

There is a strong trend of declining populations in many species of both animals and plants. Dwindling numbers of species can eventually lead to their functional extinction. Functional, or ecological, extinction occurs when a species becomes too rare to fulfill its ecological, interactive role in the ecosystem, leading to true (numerical) extinction of other depending species. Recent theoretical work on food webs suggests that the frequency of functional extinction might be surprisingly high. However, little is known about the risk of functional species extinctions in networks with other types of interactions than trophic ones. Here, we explore the frequency of functional extinctions in model ecological networks having different proportions of antagonistic and mutualistic links. Furthermore, we investigate the topological relationship between functionally and numerically extinct species. We find that (1) the frequency of functional extinctions is higher in networks containing a mixture of antagonistic and mutualistic interactions than in networks with only one type of interaction, (2) increased mortality rate of species having both mutualistic and antagonistic links is more likely to lead to extinction of another species than to extinction of the species itself compared to species having only mutualistic or antagonistic links, and (3) trophic distance (shortest path) between functionally and numerically extinct species is, on average, longer than one, indicating the importance of indirect effects. These results generalize the findings of an earlier study on food webs, demonstrating the potential importance of functional extinction in a variety of ecological network types.     

The sixth mass coextinction: are most endangered species parasites and mutualists?

The effects of species declines and extinction on biotic interactions remain poorly understood. The loss of a species is expected to result in the loss of other species that depend on it (coextinction), leading to cascading effects across trophic levels. Such effects are likely to be most severe in mutualistic and parasitic interactions. Indeed, models suggest that coextinction may be the most common form of biodiversity loss. Paradoxically, few historical or contemporary coextinction events have actually been recorded. We review the current knowledge of coextinction by: (i) considering plausible explanations for the discrepancy between predicted and observed coextinction rates; (ii) exploring the potential consequences of coextinctions; (iii) discussing the interactions and synergies between coextinction and other drivers of species loss, particularly climate change; and (iv) suggesting the way forward for understanding the phenomenon of coextinction, which may well be the most insidious threat to global biodiversity.     

Geographic structure in a widespread plant-mycorrhizal interaction: pines and false truffles

Mutualistic interactions are likely to exhibit a strong geographic mosaic in their coevolutionary dynamics, but the structure of geographic variation in these interactions is much more poorly characterized than in host-parasite interactions. We used a cross-inoculation experiment to characterize the scales and patterns at which geographic structure has evolved in an interaction between three pine species and one ectomycorrhizal fungus species along the west coast of North America. We found substantial and contrasting patterns of geographic interaction structure for the plants and fungi. The fungi exhibited a clinal pattern of local adaptation to their host plants across the geographic range of three coastal pines. In contrast, plant growth parameters were unaffected by fungal variation, but varied among plant populations and species. Both plant and fungal performance measures varied strongly with latitude. This set of results indicates that in such widespread species interactions, interacting species may evolve asymmetrically in a geographic mosaic because of differing evolutionary responses to clinally varying biotic and abiotic factors.     

Species selection and random drift in macroevolution

Species selection resulting from trait‐dependent speciation and extinction is increasingly recognized as an important mechanism of phenotypic macroevolution. However, the recent bloom in statistical methods quantifying this process faces a scarcity of dynamical theory for their interpretation, notably regarding the relative contributions of deterministic versus stochastic evolutionary forces. I use simple diffusion approximations of birth‐death processes to investigate how the expected and random components of macroevolutionary change depend on phenotype‐dependent speciation and extinction rates, as can be estimated empirically. I show that the species selection coefficient for a binary trait, and selection differential for a quantitative trait, depend not only on differences in net diversification rates (speciation minus extinction), but also on differences in species turnover rates (speciation plus extinction), especially in small clades. The randomness in speciation and extinction events also produces a species‐level equivalent to random genetic drift, which is stronger for higher turnover rates. I then show how microevolutionary processes including mutation, organismic selection, and random genetic drift cause state transitions at the species level, allowing comparison of evolutionary forces across levels. A key parameter that would be needed to apply this theory is the distribution and rate of origination of new optimum phenotypes along a phylogeny.     

Biological correlates of extinction risk in bats

We investigated patterns and processes of extinction and threat in bats using a multivariate phylogenetic comparative approach. Of nearly 1,000 species worldwide, 239 are considered threatened by the International Union for Conservation of Nature and Natural Resources (IUCN) and 12 are extinct. Small geographic ranges and low wing aspect ratios are independently found to predict extinction risk in bats, which explains 48% of the total variance in IUCN assessments of threat. The pattern and correlates of extinction risk in the two bat suborders are significantly different. A higher proportion (4%) of megachiropteran species have gone extinct in the last 500 years than microchiropteran bats (0.3%), and a higher proportion is currently at risk of extinction (Megachiroptera: 34%; Microchiroptera: 22%). While correlates of microchiropteran extinction risk are the same as in the order as a whole, megachiropteran extinction is correlated more with reproductive rate and less with wing morphology. Bat extinction risk is not randomly distributed phylogenetically: closely related species have more similar levels of threat than would be expected if extinction risk were random. Given the unbalanced nature of the evolutionary diversification of bats, it is probable that the amount of phylogenetic diversity lost if currently threatened taxa disappear may be greater than in other clades with numerically more threatened species.     

Spatial but not temporal co-divergence of a virus and its mammalian host

Co-divergence between host and parasites suggests that evolutionary processes act across similar spatial and temporal scales. Although there has been considerable work on the extent and correlates of co-divergence of RNA viruses and their mammalian hosts, relatively little is known about the extent to which virus evolution is determined by the phylogeographic history of host species. To test hypotheses related to co-divergence across a variety of spatial and temporal scales, we explored phylogenetic signatures in Andes virus (ANDV) sampled from Chile and its host rodent, Oligoryzomys longicaudatus. ANDV showed strong spatial subdivision, a phylogeographic pattern also recovered in the host using both spatial and genealogical approaches, and despite incomplete lineage sorting. Lineage structure in the virus seemed to be a response to current population dynamics in the host at the spatial scale of ecoregions. However, finer scale analyses revealed contrasting patterns of genetic structure across a latitudinal gradient. As predicted by their higher substitution rates, ANDV showed greater genealogical resolution than the rodent, with topological congruence influenced by the degree of lineage sorting within the host. However, despite these major differences in evolutionary dynamics, the geographic structure of host and virus converged across large spatial scales.