Indirect effects shape species fitness in coevolved mutualistic networks

Leandro G. Cosmo (), Ana Paula A. Assis, Marcus A. M. de Aguiar, Mathias M. Pires, Alfredo Valido, Pedro Jordano, John N. Thompson, Jordi Bascompte and Paulo R. Guimarães
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Leandro G. Cosmo: Universidade de São Paulo
Ana Paula A. Assis: Universidade de São Paulo
Marcus A. M. de Aguiar: Universidade Estadual de Campinas
Mathias M. Pires: Universidade Estadual de Campinas
Alfredo Valido: Institute of Natural Products and Agrobiology (IPNA-CSIC)
Pedro Jordano: CSIC
John N. Thompson: University of California
Jordi Bascompte: University of Zurich
Paulo R. Guimarães: Universidade de São Paulo

Nature, 2023, vol. 619, issue 7971, 788-792

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41586-023-06319-7

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