RESUMO
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.
Assuntos
Biodiversidade , Evolução Biológica , Aptidão Genética , Simbiose , Animais , Polinização , Simbiose/fisiologia , Abelhas/fisiologiaRESUMO
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.
Assuntos
Primatas , Dispersão de Sementes , Animais , Florestas , Filogenia , Plantas/genética , SimbioseRESUMO
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.
Assuntos
Evolução Biológica , Simbiose , FenótipoRESUMO
Species on Earth are interconnected with each other through ecological interactions. Defaunation can erode those connections, yet we lack evolutionary predictions about the consequences of losing interactions in human-modified ecosystems. We quantified the fate of the evolutionary history of avian-seed dispersal interactions across tropical forest fragments by combining the evolutionary distinctness of the pairwise-partner species, a proxy to their unique functional features. Both large-seeded plant and large-bodied bird species showed the highest evolutionary distinctness. We estimate a loss of 3.5 to 4.7 × 104 million years of cumulative evolutionary history of interactions due to defaunation. Bird-driven local extinctions mainly erode the most evolutionarily distinct interactions. However, the persistence of less evolutionarily distinct bird species in defaunated areas exerts a phylogenetic rescue effect through seed dispersal of evolutionarily distinct plant species.
Assuntos
Aves/fisiologia , Plantas/genética , Dispersão de Sementes/fisiologia , Sementes/fisiologia , Animais , Evolução Biológica , Ecossistema , Florestas , Humanos , FilogeniaRESUMO
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.
Assuntos
Formigas , Animais , Brasil , Ecologia , Ecossistema , PlantasRESUMO
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.
Assuntos
Florestas , Dispersão de Sementes , Animais , Aves , Ecossistema , Sementes , ÁrvoresRESUMO
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.
Assuntos
Evolução Biológica , Ecossistema , Simbiose , Animais , Formigas/fisiologia , Plantas , PolinizaçãoRESUMO
The data set provided here includes 8,320 frugivory interactions (records of pairwise interactions between plant and frugivore species) reported for the Atlantic Forest. The data set includes interactions between 331 vertebrate species (232 birds, 90 mammals, 5 fishes, 1 amphibian, and 3 reptiles) and 788 plant species. We also present information on traits directly related to the frugivory process (endozoochory), such as the size of fruits and seeds and the body mass and gape size of frugivores. Data were extracted from 166 published and unpublished sources spanning from 1961 to 2016. While this is probably the most comprehensive data set available for a tropical ecosystem, it is arguably taxonomically and geographically biased. The plant families better represented are Melastomataceae, Myrtaceae, Moraceae, Urticaceae, and Solanaceae. Myrsine coriacea, Alchornea glandulosa, Cecropia pachystachya, and Trema micrantha are the plant species with the most animal dispersers (83, 76, 76, and 74 species, respectively). Among the animal taxa, the highest number of interactions is reported for birds (3,883) followed by mammals (1,315). The woolly spider monkey or muriqui, Brachyteles arachnoides, and Rufous-bellied Thrush, Turdus rufiventris, are the frugivores with the most diverse fruit diets (137 and 121 plants species, respectively). The most important general patterns that we note are that larger seeded plant species (>12 mm) are mainly eaten by terrestrial mammals (rodents, ungulates, primates, and carnivores) and that birds are the main consumers of fruits with a high concentration of lipids. Our data set is geographically biased, with most interactions recorded for the southeast Atlantic Forest.
Assuntos
Comportamento Alimentar , Florestas , Fungos , Animais , Aves , Frutas , Herbivoria , PlantasRESUMO
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.
Assuntos
Evolução Biológica , Ecossistema , Extinção Biológica , Simbiose , Animais , Modelos BiológicosRESUMO
Species-specific traits constrain the ways organisms interact in nature. Some pairwise interactions among coexisting species simply do not occur; they are impossible to observe despite the fact that partners coexist in the same place. The author discusses these 'forbidden links' of species interaction networks. Photo: a sphingid moth, Manduca sexta visiting a flower of Tocoyena formosa (Rubiaceae) in the Brazilian Cerrado; tongue and corolla tube lengths approximately 100 mm. Courtesy of Felipe Amorim. Sazatornil, F.D., Moré, M., Benitez-Vieyra, S., Cocucci, A.A., Kitching, I.J., Schlumpberger, B.O., Oliveira, P.E., Sazima, M. & Amorim, F.W. (2016) Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks. Journal of Animal Ecology, 85, 1586-1594. Species-specific traits and life-history characteristics constrain the ways organisms interact in nature. For example, gape-limited predators are constrained in the sizes of prey they can handle and efficiently consume. When we consider the ubiquity of such constrains, it is evident how hard it can be to be a generalist partner in ecological interactions: a free-living animal or plant cannot simply interact with every available partner it encounters. Some pairwise interactions among coexisting species simply do not occur; they are impossible to observe despite the fact that partners coexist in the same place. Sazatornil et al. () explore the nature of such constraints in the mutualisms among hawkmoths and the plants they pollinate. In this iconic interaction, used by Darwin and Wallace to vividly illustrate the power of natural selection in shaping evolutionary change, both pollinators and plants are sharply constrained in their interaction modes and outcomes.