Indirect effects shape species fitness in coevolved mutualistic networks.

Ecological interactions are one of the main forces that sustain Earth's biodiversity. A major challenge for studies of ecology and evolution is to determine how these interactions affect the fitness of species when we expand from studying isolated, pairwise interactions to include networks of interacting species1-4. In networks, chains of effects caused by a range of species have an indirect effect on other species they do not interact with directly, potentially affecting the fitness outcomes of a variety of ecological interactions (such as mutualism)5-7. Here we apply analytical techniques and numerical simulations to 186 empirical mutualistic networks and show how both direct and indirect effects alter the fitness of species coevolving in these networks. Although the fitness of species usually increased with the number of mutualistic partners, most of the fitness variation across species was driven by indirect effects. We found that these indirect effects prevent coevolving species from adapting to their mutualistic partners and to other sources of selection pressure in the environment, thereby decreasing their fitness. Such decreases are distributed in a predictable way within networks: peripheral species receive more indirect effects and experience higher reductions in fitness than central species. This topological effect was also evident when we analysed an empirical study of an invasion of pollination networks by honeybees. As honeybees became integrated as a central species within networks, they increased the contribution of indirect effects on several other species, reducing their fitness. Our study shows how and why indirect effects can govern the adaptive landscape of species-rich mutualistic assemblages.

Mutualistic coevolution and community diversity favour persistence in metacommunities under environmental changes.

Linking local to regional ecological and evolutionary processes is key to understand the response of Earth's biodiversity to environmental changes. Here we integrate evolution and mutualistic coevolution in a model of metacommunity dynamics and use numerical simulations to understand how coevolution can shape species distribution and persistence in landscapes varying in space and time. Our simulations show that coevolution and species richness can synergistically shape distribution patterns by increasing colonization and reducing extinction of populations in metacommunities. Although conflicting selective pressures emerging from mutualisms may increase mismatches with the local environment and the rate of local extinctions, coevolution increases trait matching among mutualists at the landscape scale, counteracting local maladaptation and favouring colonization and range expansions. Our results show that by facilitating colonization, coevolution can also buffer the effects of environmental changes, preventing species extinctions and the collapse of metacommunities. Our findings reveal the mechanisms whereby coevolution can favour persistence under environmental changes and highlight that these positive effects are greater in more diverse systems that retain landscape connectivity.

Indirect effects drive coevolution in mutualistic networks.

Ecological interactions have been acknowledged to play a key role in shaping biodiversity. Yet a major challenge for evolutionary biology is to understand the role of ecological interactions in shaping trait evolution when progressing from pairs of interacting species to multispecies interaction networks. Here we introduce an approach that integrates coevolutionary dynamics and network structure. Our results show that non-interacting species can be as important as directly interacting species in shaping coevolution within mutualistic assemblages. The contribution of indirect effects differs among types of mutualism. Indirect effects are more likely to predominate in nested, species-rich networks formed by multiple-partner mutualisms, such as pollination or seed dispersal by animals, than in small and modular networks formed by intimate mutualisms, such as those between host plants and their protective ants. Coevolutionary pathways of indirect effects favour ongoing trait evolution by promoting slow but continuous reorganization of the adaptive landscape of mutualistic partners under changing environments. Our results show that coevolution can be a major process shaping species traits throughout ecological networks. These findings expand our understanding of how evolution driven by interactions occurs through the interplay of selection pressures moving along multiple direct and indirect pathways.

Extreme diversification of floral volatiles within and among species of Lithophragma (Saxifragaceae).

A major challenge in evolutionary biology is to understand how complex traits of multiple functions have diversified and codiversified across interacting lineages and geographic ranges. We evaluate intra- and interspecific variation in floral scent, which is a complex trait of documented importance for mutualistic and antagonistic interactions between plants, pollinators, and herbivores. We performed a large-scale, phylogenetically structured study of an entire plant genus (Lithophragma, Saxifragaceae), of which several species are coevolving with specialized pollinating floral parasites of the moth genus Greya (Prodoxidae). We sampled 94 Lithophragma populations distributed across all 12 recognized Lithophragma species and subspecies, and four populations of related saxifragaceous species. Our results reveal an unusually high diversity of floral volatiles among populations, species, and clades within the genus. Moreover, we found unexpectedly major changes at each of these levels in the biosynthetic pathways used by local populations in their floral scents. Finally, we detected significant, but variable, genus- and species-level patterns of ecological convergence in the floral scent signal, including an impact of the presence and absence of two pollinating Greya moth species. We propose that one potential key to understanding floral scent variation in this hypervariable genus is its geographically diverse interactions with the obligate specialized Greya moths and, in some species and sites, more generalized copollinators.

Annual precipitation predicts the phylogenetic signal in bat-fruit interaction networks across the Neotropics.

Closely related species tend to be more similar than randomly selected species from the same phylogenetic tree. This pattern, known as a phylogenetic signal, has been extensively studied for intrinsic (e.g. morphology), as well as extrinsic (e.g. climatic preferences), properties but less so for ecological interactions. Phylogenetic signals of species interactions (i.e. resource use) can vary across time and space, but the causes behind such variations across broader spatial extents remain elusive. Here, we evaluated how current and historical climates influence phylogenetic signals of bat-fruit interaction networks across the Neotropics. We performed a model selection relating the phylogenetic signals of each trophic level (bats and plants) with a set of current and historical climatic factors deemed ecologically important in shaping biotic interactions. Bat and plant phylogenetic signals in bat-fruit interaction networks varied little with climatic factors, although bat phylogenetic signals positively covaried with annual precipitation. These findings indicated that water availability could increase resource availability, favouring higher niche partitioning of trophic resources among bat species and hence bat phylogenetic signals across bat-fruit interaction networks. Overall, our study advances our understanding of the spatial dynamics of bat-fruit interactions by highlighting the association of current climatic factors with phylogenetic patterns of biotic interactions.

Temporal organization among pollination systems in a tropical seasonal forest.

Temporal constancy of pollination systems is essential for the maintenance of pollinators through time. Community-level assessment of flowering phenology allows understanding variations across seasons and years and the risks of decoupling flowering and pollinators' activity. We evaluated flowering patterns and temporal diversity of pollination systems in a tropical seasonal forest. We asked whether the temporal organization of flowering times differs among pollination systems; if there is a constancy of pollination systems through the year, since climate and phylogenies constraint flowering time; if there is a prevalent flowering pattern by pollination system, and if the temporal organization of pollination systems by modularity analyses is coherent with grouping by pre-defined seasons. We characterized 10 pollination systems, examined flowering strategies, climate cues and phylogenetic constraints. Pollination by large-to-medium bees dominated (49.2%), followed by diverse insects (22.1%) and flies (14.7%). The remaining systems represented 14% of species. Flowering occurred year-round for most pollination systems, predominating the seasonal flowering strategy. Flowering patterns ranged from aggregated to nested, and random. Climate affected the flowering of most pollination systems, but there was no phylogeny constraint. Modularity grouped pollination systems differently than rainfall seasonality. Contrasting the expectations of reduced temporal constancy, most systems were present year-round, facilitating the exploitation of floral resources by pollinators. Diversity of pollination systems remained constant despite climate seasonality, indicating that several factors influence the optimum flowering time for pollination in seasonally dry vegetations. Global warming may disrupt phenological patterns and the temporal organization of plant communities, a matter for future studies.

The geographic mosaic of coevolution in mutualistic networks.

Ecological interactions shape adaptations through coevolution not only between pairs of species but also through entire multispecies assemblages. Local coevolution can then be further altered through spatial processes that have been formally partitioned in the geographic mosaic theory of coevolution. A major current challenge is to understand the spatial patterns of coadaptation that emerge across ecosystems through the interplay between gene flow and selection in networks of interacting species. Here, we combine a coevolutionary model, network theory, and empirical information on species interactions to investigate how gene flow and geographical variation in selection affect trait patterns in mutualistic networks. We show that gene flow has the surprising effect of favoring trait matching, especially among generalist species in species-rich networks typical of pollination and seed dispersal interactions. Using an analytical approximation of our model, we demonstrate that gene flow promotes trait matching by making the adaptive landscapes of different species more similar to each other. We use this result to show that the progressive loss of gene flow associated with habitat fragmentation may undermine coadaptation in mutualisms. Our results therefore provide predictions of how spatial processes shape the evolution of species-rich interactions and how the widespread fragmentation of natural landscapes may modify the coevolutionary process.

Genetic correlations and ecological networks shape coevolving mutualisms.

Ecological interactions shape the evolution of multiple species traits in populations. These traits are often linked to each other through genetic correlations, affecting how each trait evolves through selection imposed by interacting partners. Here, we integrate quantitative genetics, coevolutionary theory and network science to explore how trait correlations affect the coevolution of mutualistic species not only in pairs of species but also in species-rich networks across space. We show that genetic correlations may determine the pace of coevolutionary change, affect species abundances and fuel divergence among populations of the same species. However, this trait divergence promoted by genetic correlations is partially buffered by the nested structure of species-rich mutualisms. Our study, therefore, highlights how coevolution and its ecological consequences may result from conflicting processes at different levels of organisation, ranging from genes to communities.

Associated evolution of fruit size, fruit colour and spines in Neotropical palms.

Understanding how ecological interactions have shaped the evolutionary dynamics of species traits remains a challenge in evolutionary ecology. Combining trait evolution models and phylogenies, we analysed the evolution of characters associated with seed dispersal (fruit size and colour) and herbivory (spines) in Neotropical palms to infer the role of these opposing animal-plant interactions in driving evolutionary patterns. We found that the evolution of fruit colour and fruit size was associated in Neotropical palms, supporting the adaptive interpretation of seed-dispersal syndromes and highlighting the role of frugivores in shaping plant evolution. Furthermore, we revealed a positive association between fruit size and the presence of spines on palm leaves, bracteas and stems. We hypothesize that interactions between palms and large-bodied frugivores/herbivores may explain the evolutionary relationship between fruit size and spines. Large-bodied frugivores, such as extinct megafauna, besides consuming the fruits and dispersing large seeds, may also have consumed the leaves or damaged the plants, thus simultaneously favouring the evolution of large fruits and defensive structures. Our findings show how current trait patterns can be understood as the result of the interplay between antagonistic and mutualistic interactions that have happened throughout the evolutionary history of a clade.

Coevolutionary patterns caused by prey selection.

Many theoretical models have been formulated to better understand the coevolutionary patterns that emerge from antagonistic interactions. These models usually assume that the attacks by the exploiters are random, so the effect of victim selection by exploiters on coevolutionary patterns remains unexplored. Here we analytically studied the payoff for predators and prey under coevolution assuming that every individual predator can attack only a small number of prey any given time, considering two scenarios: (i) predation occurs at random; (ii) predators select prey according to phenotype matching. We also develop an individual based model to verify the robustness of our analytical prediction. We show that both scenarios result in well known similar coevolutionary patterns if population sizes are sufficiently high: symmetrical coevolutionary branching and symmetrical coevolutionary cycling (Red Queen dynamics). However, for small population sizes, prey selection can cause unexpected coevolutionary patterns. One is the breaking of symmetry of the coevolutionary pattern, where the phenotypes evolve towards one of two evolutionarily stable patterns. As population size increases, the phenotypes oscillate between these two values in a novel form of Red Queen dynamics, the episodic reversal between the two stable patterns. Thus, prey selection causes prey phenotypes to evolve towards more extreme values, which reduces the fitness of both predators and prey, increasing the likelihood of extinction.

Coevolution Creates Complex Mosaics across Large Landscapes.

The spatial distribution of populations can influence the evolutionary outcome of species interactions. The variation in direction and strength of selection across local communities creates geographic selection mosaics that, when combined with gene flow and genomic processes such as genome duplication or hybridization, can fuel ongoing coevolution. A fundamental problem to solve is how coevolution proceeds when many populations that vary in their ecological outcomes are connected across large landscapes. Here we use a lattice model to explore this problem. Our results show that the complex interrelationships among the elements of the geographic mosaic of coevolution can lead to the formation of clusters of populations with similar phenotypes that are larger than expected by local selection. Our results indicate that neither the spatial distribution of phenotypes nor the spatial differences in magnitude and direction of selection alone dictate coevolutionary dynamics: the geographic mosaic of coevolution affects formation of phenotypic clusters, which in turn affect the spatial and temporal dynamics of coevolution. Because the formation of large phenotypic clusters depends on gene flow, we predict that current habitat fragmentation will change the outcomes of geographic mosaics, coupling spatial patterns in selection and phenotypes.

Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.

Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouring natural microbial communities, we tested whether Bd spillover from naturally infected aquatic-breeding frogs could lead to Bd amplification and mortality in our focal terrestrial-breeding host: the pumpkin toadlet Brachycephalus pitanga. We also tested whether the strength of spillover could vary depending on skin bacterial transmission within host assemblages. Terrestrial-breeding toadlets acquired lethal spillover infections from neighbouring aquatic hosts and experienced dramatic but generally non-protective shifts in skin bacterial composition primarily attributable to their Bd infections. By contrast, aquatic-breeding amphibians maintained mild Bd infections and higher survival, with shifts in bacterial microbiomes that were unrelated to Bd infections. Our results indicate that Bd spillover from even mildly infected aquatic-breeding hosts may lead to dysbiosis and mortality in terrestrial-breeding species, underscoring the need to further investigate recent population declines of terrestrial-breeding amphibians in the tropics.

Seed-dispersal interactions in fragmented landscapes - a metanetwork approach.

Mutualistic interactions repeatedly preserved across fragmented landscapes can scale-up to form a spatial metanetwork describing the distribution of interactions across patches. We explored the structure of a bird seed-dispersal (BSD) metanetwork in 16 Neotropical forest fragments to test whether a distinct subset of BSD-interactions may mediate landscape functional connectivity. The metanetwork is interaction-rich, modular and poorly connected, showing high beta-diversity and turnover of species and interactions. Interactions involving large-sized species were lost in fragments < 10 000 ha, indicating a strong filtering by habitat fragmentation on the functional diversity of BSD-interactions. Persistent interactions were performed by small-seeded, fast growing plant species and by generalist, small-bodied bird species able to cross the fragmented landscape. This reduced subset of interactions forms the metanetwork components persisting to defaunation and fragmentation, and may generate long-term deficits of carbon storage while delaying forest regeneration at the landscape level.

Eco-evolutionary feedbacks promote fluctuating selection and long-term stability of antagonistic networks.

Studies have shown the potential for rapid adaptation in coevolving populations and that the structure of species interaction networks can modulate the vulnerability of ecological systems to perturbations. Although the feedback loop between population dynamics and coevolution of traits is crucial for understanding long-term stability in ecological assemblages, modelling eco-evolutionary dynamics in species-rich assemblages is still a challenge. We explore how eco-evolutionary feedbacks influence trait evolution and species abundances in 23 empirical antagonistic networks. We show that, if selection due to antagonistic interactions is stronger than other selective pressures, eco-evolutionary feedbacks lead to higher mean species abundances and lower temporal variation in abundances. By contrast, strong selection of antagonistic interactions leads to higher temporal variation of traits and on interaction strengths. Our results present a theoretical link between the study of the species persistence and coevolution in networks of interacting species, pointing out the ways by which coevolution may decrease the vulnerability of species within antagonistic networks to demographic fluctuation.

Does biological intimacy shape ecological network structure? A test using a brood pollination mutualism on continental and oceanic islands.

Biological intimacy-the degree of physical proximity or integration of partner taxa during their life cycles-is thought to promote the evolution of reciprocal specialization and modularity in the networks formed by co-occurring mutualistic species, but this hypothesis has rarely been tested. Here, we test this "biological intimacy hypothesis" by comparing the network architecture of brood pollination mutualisms, in which specialized insects are simultaneously parasites (as larvae) and pollinators (as adults) of their host plants to that of other mutualisms which vary in their biological intimacy (including ant-myrmecophyte, ant-extrafloral nectary, plant-pollinator and plant-seed disperser assemblages). We use a novel dataset sampled from leafflower trees (Phyllanthaceae: Phyllanthus s. l. [Glochidion]) and their pollinating leafflower moths (Lepidoptera: Epicephala) on three oceanic islands (French Polynesia) and compare it to equivalent published data from congeners on continental islands (Japan). We infer taxonomic diversity of leafflower moths using multilocus molecular phylogenetic analysis and examine several network structural properties: modularity (compartmentalization), reciprocality (symmetry) of specialization and algebraic connectivity. We find that most leafflower-moth networks are reciprocally specialized and modular, as hypothesized. However, we also find that two oceanic island networks differ in their modularity and reciprocal specialization from the others, as a result of a supergeneralist moth taxon which interacts with nine of 10 available hosts. Our results generally support the biological intimacy hypothesis, finding that leafflower-moth networks (usually) share a reciprocally specialized and modular structure with other intimate mutualisms such as ant-myrmecophyte symbioses, but unlike nonintimate mutualisms such as seed dispersal and nonintimate pollination. Additionally, we show that generalists-common in nonintimate mutualisms-can also evolve in intimate mutualisms, and that their effect is similar in both types of assemblages: once generalists emerge they reshape the network organization by connecting otherwise isolated modules.

Network Structure and Selection Asymmetry Drive Coevolution in Species-Rich Antagonistic Interactions.

Ecological interactions shape and are shaped by the evolution of interacting species. Mathematical models and empirical work have explored the multiple ways coevolution could occur in small sets of species, revealing that the addition of even one species can change the coevolutionary dynamics of a pairwise interaction. As a consequence, one of the current challenges in evolutionary biology is to understand how species-rich assemblages evolve and coevolve as networks of interacting species. We combined an adaptive network framework, a trait evolutionary model, and data on network structure to study how network organization affects and is affected by selection in antagonistic interactions such as parasitism, predation, and herbivory. We explored how selection imposed by interactions shapes the evolution of attack and defense traits, parameterizing our models with structural information from 31 empirical assemblages of antagonistic species. In the simulations, the form of coevolution in antagonistic interactions is affected by the intensity and asymmetry of the selection imposed by the interacting partners. Transient escalation in attack and defensive traits was the most prevalent form of coevolutionary dynamics, especially in networks formed by modules of highly interacting species. Fluctuating evolution of traits was observed when the intensity of selection was higher in exploiters than in victims and was especially favored in nested networks. At the species level, highly connected species experienced higher temporal variation in selection regardless of the network structure, resulting in high trait mismatching with their partners. The mismatched patterns of highly connected species, in turn, may explain the emergence of modularity in antagonistic interactions in which selection is stronger on exploiters than on their victims. Our results highlight the roles of different aspects of network structure on antagonistic coevolution: nestedness shapes coevolutionary dynamics, whereas modularity emerges as one outcome of coevolutionary dynamics.

Collapse of an ecological network in Ancient Egypt.

The dynamics of ecosystem collapse are fundamental to determining how and why biological communities change through time, as well as the potential effects of extinctions on ecosystems. Here, we integrate depictions of mammals from Egyptian antiquity with direct lines of paleontological and archeological evidence to infer local extinctions and community dynamics over a 6,000-y span. The unprecedented temporal resolution of this dataset enables examination of how the tandem effects of human population growth and climate change can disrupt mammalian communities. We show that the extinctions of mammals in Egypt were nonrandom and that destabilizing changes in community composition coincided with abrupt aridification events and the attendant collapses of some complex societies. We also show that the roles of species in a community can change over time and that persistence is predicted by measures of species sensitivity, a function of local dynamic stability. To our knowledge, our study is the first high-resolution analysis of the ecological impacts of environmental change on predator-prey networks over millennial timescales and sheds light on the historical events that have shaped modern animal communities.

Unravelling Darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types.

Trying to unravel Darwin's entangled bank further, we describe the architecture of a network involving multiple forms of mutualism (pollination by animals, seed dispersal by birds and plant protection by ants) and evaluate whether this multi-network shows evidence of a structure that promotes robustness. We found that species differed strongly in their contributions to the organization of the multi-interaction network, and that only a few species contributed to the structuring of these patterns. Moreover, we observed that the multi-interaction networks did not enhance community robustness compared with each of the three independent mutualistic networks when analysed across a range of simulated scenarios of species extinction. By simulating the removal of highly interacting species, we observed that, overall, these species enhance network nestedness and robustness, but decrease modularity. We discuss how the organization of interlinked mutualistic networks may be essential for the maintenance of ecological communities, and therefore the long-term ecological and evolutionary dynamics of interactive, species-rich communities. We suggest that conserving these keystone mutualists and their interactions is crucial to the persistence of species-rich mutualistic assemblages, mainly because they support other species and shape the network organization.

Nested species-rich networks of scavenging vertebrates support high levels of interspecific competition.

Disentangling the processes that shape the organization of ecological assemblages and its implications for species coexistence is one of the foremost challenges of ecology. Although insightful advances have recently related community composition and structure with species coexistence in mutualistic and antagonistic networks, little is known regarding other species assemblages, such as those of scavengers exploiting carrion. Here we studied seven assemblages of scavengers feeding on ungulate carcasses in mainland Spain. We used dynamical models to investigate if community composition, species richness and structure (nestedness) affect species coexistence at carcasses. Scavenging networks showed a nested pattern in sites where highly efficient, obligate scavengers (i.e., vultures) were present and a non-nested pattern everywhere else. Griffon Vulture (Gyps fulvus) and certain meso-facultative mammalian scavengers (i.e., red fox, Vulpes vulpes, and stone marten, Martes foina) were the main species contributing to nestedness. Assemblages with vultures were also the richest ones in species. Nested species-rich assemblages with vulture presence were associated with high carcass consumption rates, indicating higher interspecific competition at the local scale. However, the proportion of species stopping the consumption of carrion (as derived from the competitive dynamic model) stabilized at high richness and nestedness levels. This suggests that high species richness and nestedness may characterize scavenging networks that are robust to high levels of interspecific competition for carrion. Some facilitative interactions driven by vultures and major facultative scavengers could be behind these observations. Our findings are relevant for understanding species' coexistence in highly competitive systems.

Diversification through multitrait evolution in a coevolving interaction.

Mutualisms between species are interactions in which reciprocal exploitation results in outcomes that are mutually beneficial. This reciprocal exploitation is evident in the more than a thousand plant species that are pollinated exclusively by insects specialized to lay their eggs in the flowers they pollinate. By pollinating each flower in which she lays eggs, an insect guarantees that her larval offspring have developing seeds on which to feed, whereas the plant gains a specialized pollinator at the cost of some seeds. These mutualisms are often reciprocally obligate, potentially driving not only ongoing coadaptation but also diversification. The lack of known intermediate stages in most of these mutualisms, however, makes it difficult to understand whether these interactions could have begun to diversify even before they became reciprocally obligate. Experimental studies of the incompletely obligate interactions between woodland star (Lithophragma; Saxifragaceae) plants and their pollinating floral parasites in the moth genus Greya (Prodoxidae) show that, as these lineages have diversified, the moths and plants have evolved in ways that maintain effective oviposition and pollination. Experimental assessment of pollination in divergent species and quantitative evaluation of time-lapse photographic sequences of pollination viewed on surgically manipulated flowers show that various combinations of traits are possible for maintaining the mutualism. The results suggest that at least some forms of mutualism can persist and even diversify when the interaction is not reciprocally obligate.