Climate change should drive mammal defaunation in tropical dry forests.

Human-induced climate change has intensified negative impacts on socioeconomic factors, the environment, and biodiversity, including changes in rainfall patterns and an increase in global average temperatures. Drylands are particularly at risk, with projections suggesting they will become hotter, drier, and less suitable for a significant portion of their species, potentially leading to mammal defaunation. We use ecological niche modelling and community ecology biodiversity metrics to examine potential geographical range shifts of non-volant mammal species in the largest Neotropical dryland, the Caatinga, and evaluate impacts of climate change on mammal assemblages. According to projections, 85% of the mammal species will lose suitable habitats, with one quarter of species projected to completely lose suitable habitats by 2060. This will result in a decrease in species richness for more than 90% of assemblages and an increase in compositional similarity to nearby assemblages (i.e., reduction in spatial beta diversity) for 70% of the assemblages. Small-sized mammals will be the most impacted and lose most of their suitable habitats, especially in highlands. The scenario is even worse in the eastern half of Caatinga where habitat destruction already prevails, compounding the threats faced by species there. While species-specific responses can vary with respect to dispersal, behavior, and energy requirements, our findings indicate that climate change can drive mammal assemblages to biotic homogenization and species loss, with drastic changes in assemblage trophic structure. For successful long-term socioenvironmental policy and conservation planning, it is critical that findings from biodiversity forecasts are considered.

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.

Decoupled responses of biodiversity facets driven from anuran vulnerability to climate and land-use changes.

Biodiversity loss not only implies the loss of species but also entails losses in other dimensions of biodiversity, such as functional, phylogenetic and interaction diversity. Yet, each of those facets of biodiversity may respond differently to extinctions. Here, we examine how extinction, driven by climate and land-use changes may affect those different facets of diversity by combining empirical data on anuran-prey interaction networks, species distribution modelling and extinction simulations in assemblages representing four Neotropical ecoregions. We found a mismatch in the response of functional, phylogenetic and interaction diversity to extinction. In spite of high network robustness to extinction, the effects on interaction diversity were stronger than those on phylogenetic and functional diversity, declining linearly with species loss. Although it is often assumed that interaction patterns are reflected by functional diversity, assessing species interactions may be necessary to understand how species loss translates into the loss of ecosystem functions.

Identifying climate change refugia for South American biodiversity.

Refugia-based conservation offers long-term effectiveness and minimize uncertainty on strategies for climate change adaptation. We used distribution modelling to identify climate change refugia for 617 terrestrial mammals and to quantify the role of protected areas (PAs) in providing refugia across South America. To do so, we compared species potential distribution across different scenarios of climate change, highlighting those regions likely to retain suitable climatic conditions by year 2090, and explored the proportion of refugia inside PAs. Moist tropical forests in high-elevation areas with complex topography concentrated the highest local diversity of species refugia, although regionally important refugia centers occurred elsewhere. Andean-Amazon forests contained climate change refugia for more than half of the continental species' pool and for up to 87 species locally (17 × 17 km2 grid cell). The highlands of the southern Atlantic Forest also included megadiverse refugia for up to 76 species per cell. Almost half of the species that may find refugia in the Atlantic Forest will do so in a single region-the Serra do Mar and Serra do Espinhaço. Most of the refugia we identified, however, were not in PAs, which may contain <6% of the total area of climate change refugia, leaving 129-237 species with no refugia inside the territorial limits of PAs of any kind. Our results reveal a dismal scenario for the level of refugia protection in some of the most biodiverse regions of the world. Nonetheless, because refugia tend to be in high-elevation, topographically complex, and remote areas, with lower anthropogenic pressure, formally protecting them may require a comparatively modest investment.

Identificación de refugios para la biodiversidad de Sudamérica ante el cambio climático Resumen Las estrategias de conservación basadas en refugios ofrecen efectividad a largo plazo y minimizan la incertidumbre sobre las estrategias de adaptación al cambio climático. Utilizamos modelos de distribución para identificar los refugios del cambio climático de 617 especies de mamíferos terrestres y cuantificar el papel de las áreas protegidas en la provisión de refugios en Sudamérica. Para esto, comparamos la distribución potencial de las especies en diferentes escenarios de cambio climático, destacando las regiones que probablemente conservarán las condiciones climáticas adecuadas para el año 2090, y exploramos la proporción de refugios dentro de las áreas protegidas. Los bosques tropicales húmedos de zonas de gran altitud y topografía compleja concentraron la mayor diversidad local de refugios de especies, aunque también hubo centros de refugio de importancia regional en otras localidades. Los bosques amazónicos andinos albergaron los refugios ante el cambio climático de más de la mitad del conjunto de especies continentales y para hasta 87 especies a escala local (celda cuadriculada de 17 × 17 km2 ). Las tierras altas del sur del Bosque Atlántico también incluyeron refugios megadiversos para hasta 76 especies por celda. Casi la mitad de las especies que pueden refugiarse en el Bosque Atlántico lo harán en una sola región: la Serra do Mar y la Serra do Espinhaço. Sin embargo, la mayoría de los refugios que identificamos no estaban en áreas protegidas, las cuales pueden contener <6% del área total de refugios del cambio climático, dejando entre 129 y 237 especies sin refugio dentro de los límites territoriales de las áreas protegidas de cualquier tipo. Nuestros resultados revelan un panorama desolador para el nivel de protección de los refugios en algunas de las regiones con mayor biodiversidad del mundo. No obstante, dado que los refugios suelen encontrarse en zonas remotas de gran altitud con topografía compleja y menor presión antropogénica, protegerlos formalmente puede requerir una inversión comparativamente modesta.

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.

Terrestrial food web complexity in Amazonian forests decays with habitat loss.

The conversion of natural ecosystems into human-modified landscapes (HMLs) is the main driver of biodiversity loss in terrestrial ecosystems.1,2,3 Even when species persist within habitat remnants, populations may become so small that ecological interactions are functionally lost, disrupting local interaction networks.4,5 To uncover the consequences of land use changes toward ecosystem functioning, we need to understand how changes in species richness and abundance in HMLs6,7,8 rearrange ecological networks. We used data from forest vertebrate surveys and combined modeling and network analysis to investigate how the structure of predator-prey networks was affected by habitat insularization induced by a hydroelectric reservoir in the Brazilian Amazonia.9 We found that network complexity, measured by interaction diversity, decayed non-linearly with decreasingly smaller forest area. Although on large forest islands (>100 ha) prey species were linked to 3-4 potential predators, they were linked to one or had no remaining predator on small islands. Using extinction simulations, we show that the variation in network structure cannot be explained by abundance-related extinction risk or prey availability. Our findings show that habitat loss may result in an abrupt disruption of terrestrial predator-prey networks, generating low-complexity ecosystems that may not retain functionality. Release from predation on some small islands may produce cascading effects over plants that accelerate forest degradation, whereas predator spillover on others may result in overexploited prey populations. Our analyses highlight that in addition to maintaining diversity, protecting large continuous forests is required for the persistence of interaction networks and related ecosystem functions.

Differences in prey availability across space and time lead to interaction rewiring and reshape a predator-prey metaweb.

Space and time promote variation in network structure by affecting the likelihood of potential interactions. However, little is known about the relative roles of ecological and biogeographical processes in determining how species interactions vary across space and time. Here we study the spatiotemporal variation in predator-prey interaction networks formed by anurans and arthropods and test for the effects of prey availability in determining interaction patterns, information that is often absent and limits the understanding of the determinants of network structure. We found that network dissimilarity between ecoregions and seasons was high and primarily driven by interaction rewiring.We also found that species turnover was positively related to geographical distance. Using a null model approach to disentangle the effect of prey availability on the spatial and temporal variation, we show that differences in prey availability were important in determining the variation in network structure between seasons and among areas. Our study reveals that fluctuations in prey abundance, alongside the limited dispersal abilities of anurans and their prey, may be responsible for the spatial patterns that emerged in our predator-prey metaweb. These findings contribute to our understanding of the assembly rules that maintain biotic processes in metacommunities and highlight the importance of prey availability to the structure of these systems.

The effect of past defaunation on ranges, niches, and future biodiversity forecasts.

Humans have reshaped the distribution of biodiversity across the globe, extirpating species from regions otherwise suitable and restricting populations to a subset of their original ranges. Here, we ask if anthropogenic range contractions since the Late Pleistocene led to an under-representation of the realized niches for megafauna, an emblematic group of taxa often targeted for restoration actions. Using reconstructions of past geographic distributions (i.e., natural ranges) for 146 extant terrestrial large-bodied (>44 kg) mammals, we estimate their climatic niches as if they had retained their original distributions and evaluate their observed niche dynamics. We found that range contractions led to a sizeable under-representation of the realized niches of several species (i.e., niche unfilling). For 29 species, more than 10% of the environmental space once seen in their natural ranges has been lost due to anthropogenic activity, with at least 12 species undergoing reductions of more than 50% of their realized niches. Eighteen species may now be confined to low-suitability locations, where fitness and abundance are likely diminished; we consider these taxa 'climatic refugees'. For those species, conservation strategies supported by current ranges risk being misguided if current, suboptimal habitats are considered baseline for future restoration actions. Because most climate-based biodiversity forecasts rely exclusively on current occurrence records, we went on to test the effect of neglecting historical information on estimates of species' potential distribution - as a proxy of sensitivity to climate change. We found that niche unfilling driven by past range contraction leads to an overestimation of sensitivity to future climatic change, resulting in 50% higher rates of global extinction, and underestimating the potential for megafauna conservation and restoration under future climate change. In conclusion, range contractions since the Late Pleistocene have also left imprints on megafauna realized climatic niches. Therefore, niche truncation driven by defaunation can directly affect climate and habitat-based conservation strategies.

How deregulation, drought and increasing fire impact Amazonian biodiversity.

Biodiversity contributes to the ecological and climatic stability of the Amazon Basin1,2, but is increasingly threatened by deforestation and fire3,4. Here we quantify these impacts over the past two decades using remote-sensing estimates of fire and deforestation and comprehensive range estimates of 11,514 plant species and 3,079 vertebrate species in the Amazon. Deforestation has led to large amounts of habitat loss, and fires further exacerbate this already substantial impact on Amazonian biodiversity. Since 2001, 103,079-189,755 km2 of Amazon rainforest has been impacted by fires, potentially impacting the ranges of 77.3-85.2% of species that are listed as threatened in this region5. The impacts of fire on the ranges of species in Amazonia could be as high as 64%, and greater impacts are typically associated with species that have restricted ranges. We find close associations between forest policy, fire-impacted forest area and their potential impacts on biodiversity. In Brazil, forest policies that were initiated in the mid-2000s corresponded to reduced rates of burning. However, relaxed enforcement of these policies in 2019 has seemingly begun to reverse this trend: approximately 4,253-10,343 km2 of forest has been impacted by fire, leading to some of the most severe potential impacts on biodiversity since 2009. These results highlight the critical role of policy enforcement in the preservation of biodiversity in the Amazon.

Climate and land-use change will lead to a faunal "savannization" on tropical rainforests.

Humans have fragmented, reduced or altered the biodiversity in tropical forests around the world. Climate and land-use change act synergistically, increasing drought and fire frequencies, converting several tropical rainforests into derived savannas, a phenomenon known as "savannization." Yet, we lack a full understanding of the faunal changes in response to the transformation of plant communities. We argue that the composition of vertebrate assemblages in ecotone regions of forest-savanna transitions from South America will be increasingly replaced by open savanna species, a phenomenon we name "faunal savannization." We combined projections from ecological niche models, habitat filter masks and dispersal simulations to forecast the distribution of 349 species of forest- and savanna-dwelling mammal species across South America. We found that the distribution of savanna species is likely to increase by 11%-30% and spread over lowland Amazon and Atlantic forests. Conversely, forest-specialists are expected to lose nearly 50% of their suitable ranges and to move toward core forest zones, which may thus receive an influx of more than 60 species on the move. Our findings indicate that South American ecotonal faunas might experience high rates of occupancy turnover, in a process parallel to that already experienced by plants. Climate-driven migrations of fauna in human-dominated landscapes will likely interact with fire-induced changes in plant communities to reshape the biodiversity in tropical rainforests worldwide.

Diverse interactions and ecosystem engineering can stabilize community assembly.

The complexity of an ecological community can be distilled into a network, where diverse interactions connect species in a web of dependencies. Species interact directly with each other and indirectly through environmental effects, however to our knowledge the role of these ecosystem engineers has not been considered in ecological network models. Here we explore the dynamics of ecosystem assembly, where species colonization and extinction depends on the constraints imposed by trophic, service, and engineering dependencies. We show that our assembly model reproduces many key features of ecological systems, such as the role of generalists during assembly, realistic maximum trophic levels, and increased nestedness with mutualistic interactions. We find that ecosystem engineering has large and nonlinear effects on extinction rates. While small numbers of engineers reduce stability by increasing primary extinctions, larger numbers of engineers increase stability by reducing primary extinctions and extinction cascade magnitude. Our results suggest that ecological engineers may enhance community diversity while increasing persistence by facilitating colonization and limiting competitive exclusion.

The indirect paths to cascading effects of extinctions in mutualistic networks.

Biodiversity loss is a hallmark of our times, but predicting its consequences is challenging. Ecological interactions form complex networks with multiple direct and indirect paths through which the impacts of an extinction may propagate. Here we show that accounting for these multiple paths connecting species is necessary to predict how extinctions affect the integrity of ecological networks. Using an approach initially developed for the study of information flow, we estimate indirect effects in plant-pollinator networks and find that even those species with several direct interactions may have much of their influence over others through long indirect paths. Next, we perform extinction simulations in those networks and show that although traditional connectivity metrics fail in the prediction of coextinction patterns, accounting for indirect interaction paths allows predicting species' vulnerability to the cascading effects of an extinction event. Embracing the structural complexity of ecological systems contributes towards a more predictive ecology, which is of paramount importance amid the current biodiversity crisis.

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.

Revealing biases in the sampling of ecological interaction networks.

The structure of ecological interactions is commonly understood through analyses of interaction networks. However, these analyses may be sensitive to sampling biases with respect to both the interactors (the nodes of the network) and interactions (the links between nodes), because the detectability of species and their interactions is highly heterogeneous. These ecological and statistical issues directly affect ecologists' abilities to accurately construct ecological networks. However, statistical biases introduced by sampling are difficult to quantify in the absence of full knowledge of the underlying ecological network's structure. To explore properties of large-scale ecological networks, we developed the software EcoNetGen, which constructs and samples networks with predetermined topologies. These networks may represent a wide variety of communities that vary in size and types of ecological interactions. We sampled these networks with different mathematical sampling designs that correspond to methods used in field observations. The observed networks generated by each sampling process were then analyzed with respect to the number of components, size of components and other network metrics. We show that the sampling effort needed to estimate underlying network properties depends strongly both on the sampling design and on the underlying network topology. In particular, networks with random or scale-free modules require more complete sampling to reveal their structure, compared to networks whose modules are nested or bipartite. Overall, modules with nested structure were the easiest to detect, regardless of the sampling design used. Sampling a network starting with any species that had a high degree (e.g., abundant generalist species) was consistently found to be the most accurate strategy to estimate network structure. Because high-degree species tend to be generalists, abundant in natural communities relative to specialists, and connected to each other, sampling by degree may therefore be common but unintentional in empirical sampling of networks. Conversely, sampling according to module (representing different interaction types or taxa) results in a rather complete view of certain modules, but fails to provide a complete picture of the underlying network. To reduce biases introduced by sampling methods, we recommend that these findings be incorporated into field design considerations for projects aiming to characterize large species interaction networks.

Analysing ecological networks of species interactions.

Network approaches to ecological questions have been increasingly used, particularly in recent decades. The abstraction of ecological systems - such as communities - through networks of interactions between their components indeed provides a way to summarize this information with single objects. The methodological framework derived from graph theory also provides numerous approaches and measures to analyze these objects and can offer new perspectives on established ecological theories as well as tools to address new challenges. However, prior to using these methods to test ecological hypotheses, it is necessary that we understand, adapt, and use them in ways that both allow us to deliver their full potential and account for their limitations. Here, we attempt to increase the accessibility of network approaches by providing a review of the tools that have been developed so far, with - what we believe to be - their appropriate uses and potential limitations. This is not an exhaustive review of all methods and metrics, but rather, an overview of tools that are robust, informative, and ecologically sound. After providing a brief presentation of species interaction networks and how to build them in order to summarize ecological information of different types, we then classify methods and metrics by the types of ecological questions that they can be used to answer from global to local scales, including methods for hypothesis testing and future perspectives. Specifically, we show how the organization of species interactions in a community yields different network structures (e.g., more or less dense, modular or nested), how different measures can be used to describe and quantify these emerging structures, and how to compare communities based on these differences in structures. Within networks, we illustrate metrics that can be used to describe and compare the functional and dynamic roles of species based on their position in the network and the organization of their interactions as well as associated new methods to test the significance of these results. Lastly, we describe potential fruitful avenues for new methodological developments to address novel ecological questions.

Interaction paths promote module integration and network-level robustness of spliceosome to cascading effects.

The functionality of distinct types of protein networks depends on the patterns of protein-protein interactions. A problem to solve is understanding the fragility of protein networks to predict system malfunctioning due to mutations and other errors. Spectral graph theory provides tools to understand the structural and dynamical properties of a system based on the mathematical properties of matrices associated with the networks. We combined two of such tools to explore the fragility to cascading effects of the network describing protein interactions within a key macromolecular complex, the spliceosome. Using S. cerevisiae as a model system we show that the spliceosome network has more indirect paths connecting proteins than random networks. Such multiplicity of paths may promote routes to cascading effects to propagate across the network. However, the modular network structure concentrates paths within modules, thus constraining the propagation of such cascading effects, as indicated by analytical results from the spectral graph theory and by numerical simulations of a minimal mathematical model parameterized with the spliceosome network. We hypothesize that the concentration of paths within modules favors robustness of the spliceosome against failure, but may lead to a higher vulnerability of functional subunits, which may affect the temporal assembly of the spliceosome. Our results illustrate the utility of spectral graph theory for identifying fragile spots in biological systems and predicting their implications.

Estimating interaction credit for trophic rewilding in tropical forests.

Trophic rewilding has been suggested as a restoration tool to restore ecological interactions and reverse defaunation and its cascading effects on ecosystem functioning. One of the ecological processes that has been jeopardized by defaunation is animal-mediated seed dispersal. Here, we propose an approach that combines joint species distribution models with occurrence data and species interaction records to quantify the potential to restore seed-dispersal interactions through rewilding and apply it to the Atlantic Forest, a global biodiversity hotspot. Using this approach, we identify areas that should benefit the most from trophic rewilding and candidate species that could contribute to cash the credit of seed-dispersal interactions in a given site. We found that sites within large fragments bearing a great diversity of trees may have about 20 times as many interactions to be cashed through rewilding as small fragments in regions where deforestation has been pervasive. We also ranked mammal and bird species according to their potential to restore seed-dispersal interactions if reintroduced while considering the biome as a whole and at finer scales. The suggested approach can aid future conservation efforts in rewilding projects in defaunated tropical rainforests.This article is part of the theme issue 'Trophic rewilding: consequences for ecosystems under global change'.

Diversification dynamics of mammalian clades during the K-Pg mass extinction.

The Cretaceous/Palaeogene (K-Pg) episode is an iconic mass extinction, in which the diversity of numerous clades abruptly declined. However, the responses of individual clades to mass extinctions may be more idiosyncratic than previously understood. Here, we examine the diversification dynamics of the three major mammalian clades in North America across the K-Pg. Our results show that these clades responded in dramatically contrasting ways to the K-Pg event. Metatherians underwent a sudden rise in extinction rates shortly after the K-Pg, whereas declining origination rates first halted diversification and later drove the loss of diversity in multituberculates. Eutherians experienced high taxonomic turnover near the boundary, with peaks in both origination and extinction rates. These findings indicate that the effects of geological episodes on diversity are context dependent and that mass extinctions can affect the diversification of clades by independently altering the extinction regime, the origination regime or both.

Ecological and evolutionary legacy of megafauna extinctions.

For hundreds of millions of years, large vertebrates (megafauna) have inhabited most of the ecosystems on our planet. During the late Quaternary, notably during the Late Pleistocene and the early Holocene, Earth experienced a rapid extinction of large, terrestrial vertebrates. While much attention has been paid to understanding the causes of this massive megafauna extinction, less attention has been given to understanding the impacts of loss of megafauna on other organisms with whom they interacted. In this review, we discuss how the loss of megafauna disrupted and reshaped ecological interactions, and explore the ecological consequences of the ongoing decline of large vertebrates. Numerous late Quaternary extinct species of predators, parasites, commensals and mutualistic partners were associated with megafauna and were probably lost due to their strict dependence upon them (co-extinctions). Moreover, many extant species have megafauna-adapted traits that provided evolutionary benefits under past megafauna-rich conditions, but are now of no or limited use (anachronisms). Morphological evolution and behavioural changes allowed some of these species partially to overcome the absence of megafauna. Although the extinction of megafauna led to a number of co-extinction events, several species that likely co-evolved with megafauna established new interactions with humans and their domestic animals. Species that were highly specialized in interactions with megafauna, such as large predators, specialized parasites, and large commensalists (e.g. scavengers, dung beetles), and could not adapt to new hosts or prey were more likely to die out. Partners that were less megafauna dependent persisted because of behavioural plasticity or by shifting their dependency to humans via domestication, facilitation or pathogen spill-over, or through interactions with domestic megafauna. We argue that the ongoing extinction of the extant megafauna in the Anthropocene will catalyse another wave of co-extinctions due to the enormous diversity of key ecological interactions and functional roles provided by the megafauna.

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.