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.

Coevolutionary hotspots favour dispersal and fuel biodiversity in mutualistic landscapes under environmental changes.

Mutualistic interactions are key to sustaining Earth's biodiversity. Yet, we are only beginning to understand how coevolution in mutualistic assemblages can shape the distribution and persistence of species across landscapes. Here, we combine the geographic mosaic theory of coevolution with metacommunity dynamics to understand how geographically structured selection can shape patterns of richness, dispersal, extinction and persistence of mutualistic species. In this model, species may experience strong or weak reciprocal selection imposed by mutualisms within each patch (i.e. hotspots and coldspots, respectively). Using numerical simulations, we show that mutualistic coevolution leads to a concentration of species richness at hotspots. Such an effect occurs because hotspots sustain higher rates of colonization and lower rates of extinction than coldspots, whether the environment changes or not. Importantly, under environmental changes, coldspots fail to sustain a positive colonization-to-extinction balance. Rather, species persistence within coldspots relies on hotspots acting as biodiversity sources and enhancing population dispersal across the landscape. In fact, even a few hotspots in the landscape can fuel the spatial network of dispersal of populations in the metacommunity. Our study highlights that coevolutionary hotspots can act as biodiversity sources, favouring colonization and allowing species to expand their distribution across landscapes even in changing environments. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

The Ecology of Plant Chemistry and Multi-Species Interactions in Diversified Agroecosystems.

Over the past few years, our knowledge of how ecological interactions shape the structure and dynamics of natural communities has rapidly advanced. Plant chemical traits play key roles in these processes because they mediate a diverse range of direct and indirect interactions in a community-wide context. Many chemically mediated interactions have been extensively studied in industrial cropping systems, and thus have focused on simplified, pairwise and linear interactions that rarely incorporate a community perspective. A contrasting approach considers the agroecosystem as a functioning whole, in which food production occurs. It offers an opportunity to better understand how plant chemical traits mediate complex interactions which can enhance or hinder ecosystem functions. In this paper, we argue that studying chemically mediated interactions in agroecosystems is essential to comprehend how agroecosystem services emerge and how they can be guaranteed through ecosystem management. First, we discuss how plant chemical traits affect and are affected by ecological interactions. We then explore research questions and future directions on how studying chemical mediation in complex agroecosystems can help us understand the emergence and management of ecosystem services, specifically biological control and pollination.