Indirect effects drive coevolution in mutualistic networks


Ecological interactions have been acknowledged to play a key role in shaping biodiversity1,2. 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 networks2. 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.

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Figure 1: Mutualisms, selection, and trait distributions.
Figure 2: Direct and indirect effects in networks.
Figure 3: Determinants of indirect effects.
Figure 4: Indirect effects and environmental change.


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We thank J. Bronstein, G. Marroig, M. A. M. de Aguiar, S. F. dos Reis, F. M. D. Marquitti, P. Lemos-Costa, L. P. Medeiros, T. Quental, R. Cogni, and the members of the Guimarães laboratory for providing suggestions at different stages of this study. P.R.G. was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (2016/20739-9) and CNPq. M.M.P. was supported by FAPESP (2013/22016-6). J.B. was supported by the European Research Council through an Advanced Grant and by the Swiss National Science Foundation (31003A_160671). P.J. was supported by a Severo Ochoa Excellence Award (SEV-2012-0262; Spanish Ministerio de Ciencia e Innovación).

Author information




All authors designed the study. P.R.G. performed the simulations and developed the analytical approximations of the model. P.R.G. and M.M.P. analysed the simulations. P.R.G., J.N.T., and J.B. wrote a first draft of the manuscript, and all authors contributed substantially to the final draft.

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Correspondence to Paulo R. Guimarães Jr.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks T. Ohgushi and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Trait dynamics of a mutualistic network.

a, A typical simulation of the coevolutionary model describing the temporal variation in the trait dynamics for a four-species network (b, see also Fig. 1c). Points of a given colour represent the evolution of the mean trait value of one species. Small squares indicate the environmental optima of the species in the network. Squares and points corresponding to the same species are presented in the same colour. The mean mutualistic selection was set at <m> = 0.7 ± 0.01. Other parameters: φ = 0.2 ± 0.01, θi = U[0, 10]. Similarly, the simulations converged to equilibrium for all empirical networks.

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Supplementary Information

This file contains Supplementary Methods describing the modeling approach, the analytical approximation, sensitivity analysis, and statistical analysis and Supplementary Tables 1-4. (PDF 1208 kb)

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Guimarães, P., Pires, M., Jordano, P. et al. Indirect effects drive coevolution in mutualistic networks. Nature 550, 511–514 (2017).

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