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.

Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

Highly clustered mating networks in naturally fragmented riparian tree populations.

Understanding how spatial patterns of mating and gene flow respond to habitat loss and geographical isolation is a crucial aspect of forest fragmentation genetics. Naturally fragmented riparian tree populations exhibit unique characteristics that significantly influence these patterns. In this study, we investigate mating patterns, pollen-mediated gene flow, and genetic diversity in relict populations of Frangula alnus in southern Spain by testing specific hypotheses related to the riparian habitat. We employ a novel approach that combines paternity analysis, particularly suited for small and isolated populations, with complex network theory and Bayesian models to predict mating likelihood among tree pairs. Our findings reveal a prevalence of short-distance pollination, resulting in spatially driven local mating clusters with a distinct subset of trees being highly connected in the mating network. Additionally, we observe numerous pollination events over distances of hundreds of metres and considerable pollen immigration. Local neighbourhood density is the primary factor influencing within-population mating patterns and pollen dispersal; moreover, mating network properties reflect the population's size and spatial configuration. Conversely, among-population pollen dispersal is mainly determined by tree size, which influences floral display. Our results do not support a major role of directional pollen dispersal in longitudinal trends of genetic diversity. We provide evidence that long-term fragmented tree populations persist in unique environments that shape mating patterns and impose constraints to pollen-mediated gene flow. Nevertheless, even seemingly strongly isolated populations can maintain functional connectivity over extended periods, especially when animal-mediated mating networks promote genetic diversity, as in this riparian tree species.

Intraspecific variation in species interactions promotes the feasibility of mutualistic assemblages.

Patterns of resource use observed at the species level emerge from the way individuals exploit the range of available resources. Hence, accounting for interindividual differences in resource use, such as pollinator use by plants, is essential to advance our understanding of community assembly and persistence. By using finely resolved data on plant-pollinator interactions, we evaluated how interindividual plant variation in pollinator use scales up to affect community structure and dynamics. All co-occurring plant species comprised specialists interacting with proper subsets of pollinators that visited generalists, and differences in interaction patterns were driven by among-individual trait variation. Furthermore, the nested structure and feasibility of plant-pollinator communities were maximised at higher levels of interindividual plant variation in traits and pollinator use. Our study sheds light on how pervasive properties of community structure arise from individual-level processes and contributes to elucidate the importance of preserving intraspecific variation in traits and resource use within populations.

Reciprocity and interaction effectiveness in generalised mutualisms among free-living species.

Mutualistic interactions among free-living species generally involve low-frequency interactions and highly asymmetric dependence among partners, yet our understanding of factors behind their emergence is still limited. Using individual-based interactions of a super-generalist fleshy-fruited plant with its frugivore assemblage, we estimated the Resource Provisioning Effectiveness (RPE) and Seed Dispersal Effectiveness (SDE) to assess the balance in the exchange of resources. Plants were highly dependent on a few frugivore species, while frugivores interacted with most individual plants, resulting in strong asymmetries of mutual dependence. Interaction effectiveness was mainly driven by interaction frequency. Despite highly asymmetric dependences, the strong reliance on quantity of fruit consumed determined high reciprocity in rewards between partners (i.e. higher energy provided by the plant, more seedlings recruited), which was not obscured by minor variations in the quality of animal or plant service. We anticipate reciprocity will emerge in low-intimacy mutualisms where the mutualistic outcome largely relies upon interaction frequency.

The turnover of plant-frugivore interactions along plant range expansion: consequences for natural colonization processes.

Plant-animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant-frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes.

Founder events and subsequent genetic bottlenecks underlie karyotype evolution in the Ibero - North African endemic Carex helodes.

BACKGROUND AND AIMS: Despite chromosomal evolution being one of the major drivers of diversification in plants, we do not yet have a clear view of how new chromosome rearrangements become fixed within populations, which is a crucial step forward for understanding chromosomal speciation. METHODS: In this study, we test the role of genetic drift in the establishment of new chromosomal variants in the context of hybrid dysfunction models of chromosomal speciation. We genotyped a total of 178 individuals from seven populations (plus 25 seeds from one population) across the geographic range of Carex helodes (Cyperaceae). We also characterized karyotype geographic patterns of the species across the distribution range. For one of the populations, we performed a detailed study of the fine scale, local spatial distribution of its individuals and their genotypes and karyotypes. KEY RESULTS: Synergistically, phylogeographic and karyotypic evidence show two main genetic groups: southwestern Iberian Peninsula vs. northwestern African populations, and within Europe our results suggest a west-to-east expansion with signals of genetic bottlenecks. Additionally, we have inferred a pattern of descending dysploidy, plausibly as a result of a west-to-east process of post-glacial colonization in Europe. CONCLUSIONS: Our results give experimental support to the role of geographic isolation, drift, and inbreeding in the establishment of new karyotypes which is key in the speciation models of hybrid dysfunction.

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.

The ecological and evolutionary significance of effectiveness landscapes in mutualistic interactions.

Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (quantity component) multiplied by the probability that an immediate outcome results in a new individual (quality component). These components form a two-dimensional effectiveness landscape with each species' location determined by its values of quantity (x-axis) and quality (y-axis). We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness values: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components. We illustrate this approach using a large dataset on synzoochory, seed dispersal by seed-caching animals. The synzoochory landscape was clumped, with effectiveness determined primarily by the quality component, and with quantity and quality positively correlated. We suggest this type of landscape structure is common in generalised coevolved mutualisms, where multiple functionally equivalent, high-quality partners exert similarly strong selection. Presumably, only those organisms located in high-quality regions will impact the evolution of their partner. Exploring properties of effectiveness landscapes in other mutualisms will provide new insight into the evolutionary and ecological consequences of mutualisms.

Phylogenetic congruence between Neotropical primates and plants is driven by frugivory.

Seed dispersal benefits plants and frugivores, and potentially drives co-evolution, with consequences to diversification evidenced for, e.g., primates. Evidence for macro-coevolutionary patterns in multi-specific, plant-animal mutualisms is scarce, and the mechanisms driving them remain unexplored. We tested for phylogenetic congruences in primate-plant interactions and showed strong co-phylogenetic signals across Neotropical forests, suggesting that both primates and plants share evolutionary history. Phylogenetic congruence between Platyrrhini and Angiosperms was driven by the most generalist primates, modulated by their functional traits, interacting with a wide-range of Angiosperms. Consistently similar eco-evolutionary dynamics seem to be operating irrespective of local assemblages, since co-phylogenetic signal emerged independently across three Neotropical regions. Our analysis supports the idea that macroevolutionary, coevolved patterns among interacting mutualistic partners are driven by super-generalist taxa. Trait convergence among multiple partners within multi-specific assemblages appears as a mechanism favouring these likely coevolved outcomes.

Species-area and network-area relationships in host-helminth interactions.

The scaling relationship observed between species richness and the geographical area sampled (i.e. the species-area relationship (SAR)) is a widely recognized macroecological relationship. Recently, this theory has been extended to trophic interactions, suggesting that geographical area may influence the structure of species interaction networks (i.e. network-area relationships (NARs)). Here, we use a global dataset of host-helminth parasite interactions to test existing predictions from macroecological theory. Scaling between single locations to the global host-helminth network by sequentially adding networks together, we find support that geographical area influences species richness and the number of species interactions in host-helminth networks. However, species-area slopes were larger for host species relative to their helminth parasites, counter to theoretical predictions. Lastly, host-helminth network modularity-capturing the tendency of the network to form into separate subcommunities-decreased with increasing area, also counter to theoretical predictions. Reconciling this disconnect between existing theory and observed SAR and NAR will provide insight into the spatial structuring of ecological networks, and help to refine theory to highlight the effects of network type, species distributional overlap, and the specificity of trophic interactions on NARs.

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.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

The timing of frugivore-mediated seed dispersal effectiveness.

The seed dispersal effectiveness framework allows assessing mutualistic services from frugivorous animals in terms of quantity and quality. Quantity accounts for the number of seeds dispersed and quality for the probability of recruitment of dispersed seeds. Research on this topic has largely focused on the spatial patterns of seed deposition because seed fates often vary between microhabitats due to differences in biotic and abiotic factors. However, the temporal dimension has remained completely overlooked despite these factors-and even local disperser assemblages-can change dramatically during long fruiting periods. Here, we test timing effects on seed dispersal effectiveness, using as study case a keystone shrub species dispersed by frugivorous birds and with a fruiting period of 9 months. We evaluated quantity and quality in different microhabitats of a Mediterranean forest and different periods of the fruiting phenophase. We identified the bird species responsible for seed deposition through DNA barcoding and evaluated the probability of seedling recruitment through a series of field experiments on sequential demographic processes. We found that timing matters: The disperser assemblage was temporally structured, seed viability decreased markedly during the plant's fruiting phenophase, and germination was lower for viable seeds dispersed in the fruiting peak. We show how small contributions to seed deposition by transient migratory species can result in a relevant effectiveness if they disperse seeds in a high-quality period for seedling recruitment. This study expands our understanding of seed dispersal effectiveness, highlighting the importance of timing and infrequent interactions for population and community dynamics.

Chasing Ecological Interactions.

Basic research on biodiversity has concentrated on individual species-naming new species, studying distribution patterns, and analyzing their evolutionary relationships. Yet biodiversity is more than a collection of individual species; it is the combination of biological entities and processes that support life on Earth. To understand biodiversity we must catalog it, but we must also assess the ways species interact with other species to provide functional support for the Tree of Life. Ecological interactions may be lost well before the species involved in those interactions go extinct; their ecological functions disappear even though they remain. Here, I address the challenges in studying the functional aspects of species interactions and how basic research is helping us address the fast-paced extinction of species due to human activities.

The influence of spatial sampling scales on ant-plant interaction network architecture.

Despite great interest in metrics to quantify the structure of ecological networks, the effects of sampling and scale remain poorly understood. In fact, one of the most challenging issues in ecology is how to define suitable scales (i.e., temporal or spatial) to accurately describe and understand ecological systems. Here, we sampled a series of ant-plant interaction networks in the southern Brazilian Amazon rainforest in order to determine whether the spatial sampling scale, from local to regional, affects our understanding of the structure of these networks. To this end, we recorded ant-plant interactions in adjacent 25 × 30 m subplots (local sampling scale) nested within twelve 250 × 30 m plots (regional sampling scale). Moreover, we combined adjacent or random subplots and plots in order to increase the spatial sampling scales at the local and regional levels. We then calculated commonly used binary and quantitative network-level metrics for both sampling scales (i.e., number of species and interactions, nestedness, specialization and modularity), all of which encompass a wide array of structural patterns in interaction networks. We observed increasing species and interactions across sampling scales, and while most network descriptors remained relatively constant at the local level, there was more variation at the regional scale. Among all metrics, specialization was most constant across different spatial sampling scales. Furthermore, we observed that adjacent assembly did not generate more variation in network descriptor values compared to random assembly. This finding indicates that the spatially aggregated distribution of species/individuals and abiotic conditions does not affect the organization of these interacting assemblages. Our results have a direct impact on our empirical and theoretical understanding of the ecological dynamics of species interactions by demonstrating that small spatial sampling scales should suffice to record some patterns commonly found in ant-plant interaction networks in a highly diverse tropical rainforest.

Seed dispersal by dispersing juvenile animals: a source of functional connectivity in fragmented landscapes.

Juvenile animals generally disperse from their birthplace to their future breeding territories. In fragmented landscapes, habitat-specialist species must disperse through the anthropogenic matrix where remnant habitats are embedded. Here, we test the hypothesis that dispersing juvenile frugivores leave a footprint in the form of seed deposition through the matrix of fragmented landscapes. We focused on the Sardinian warbler ( Sylvia melanocephala), a resident frugivorous passerine. We used data from field sampling of bird-dispersed seeds in the forest and matrix of a fragmented landscape, subsequent disperser identification through DNA-barcoding analysis, and data from a national bird-ringing programme. Seed dispersal by Sardinian warblers was confined to the forest most of the year, but warblers contributed a peak of seed-dispersal events in the matrix between July and October, mainly attributable to dispersing juveniles. Our study uniquely connects animal and plant dispersal, demonstrating that juveniles of habitat-specialist frugivores can provide mobile-link functions transiently, but in a seasonally predictable way.

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.

Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant-frugivore networks.

There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.