Indirect effects drive coevolution in mutualistic networks

Abstract

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.

References

  1. 1

    Ehrlich, P. R. & Raven, P. H. Butterflies and plants: a study in coevolution. Evolution 18, 586–608 (1964)

    Article  Google Scholar 

  2. 2

    Thompson, J. N. The Geographic Mosaic of Coevolution (Univ. Chicago Press, 2005)

  3. 3

    Galetti, M. et al. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090 (2013)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Koskella, B. & Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916–931 (2014)

    CAS  Article  Google Scholar 

  5. 5

    Parchman, T. L. & Benkman, C. W. Diversifying coevolution between crossbills and black spruce on Newfoundland. Evolution 56, 1663–1672 (2002)

    Article  Google Scholar 

  6. 6

    Brodie, E. D. III . Genetic correlations between morphology and antipredator behaviour in natural populations of the garter snake Thamnophis ordinoides. Nature 342, 542–543 (1989)

    ADS  Article  Google Scholar 

  7. 7

    Ridenhour, B. J. Identification of selective sources: partitioning selection based on interactions. Am. Nat. 166, 12–25 (2005)

    Article  Google Scholar 

  8. 8

    Strauss, S. Y., Sahli, H. & Conner, J. K. Toward a more trait-centered approach to diffuse (co)evolution. New Phytol. 165, 81–90 (2005)

    Article  Google Scholar 

  9. 9

    Iwao, K. & Rausher, M. D. Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am. Nat. 149, 316–335 (1997)

    Article  Google Scholar 

  10. 10

    Thompson, J. N., Schwind, C., Guimarães, P. R. Jr & Friberg, M. Diversification through multitrait evolution in a coevolving interaction. Proc. Natl Acad. Sci. USA 110, 11487–11492 (2013)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Fox, L. R. Diffuse coevolution within complex communities. Ecology 69, 906–907 (1988)

    Article  Google Scholar 

  12. 12

    Ohgushi, T ., Schmitz, O. & Holt, R. D. Trait-Mediated Indirect Interactions: Ecological and Evolutionary Perspectives (Cambridge Univ. Press, 2012)

  13. 13

    Gómez, J. M., Perfectti, F., Bosch, J. & Camacho, J. P. M. A geographic selection mosaic in a generalized plant-pollinator-herbivore system. Ecol. Monogr. 79, 245–263 (2009)

    Article  Google Scholar 

  14. 14

    Nuismer, S. L., Jordano, P. & Bascompte, J. Coevolution and the architecture of mutualistic networks. Evolution 67, 338–354 (2013)

    Article  Google Scholar 

  15. 15

    Santamaría, L. & Rodríguez-Gironés, M. A. Linkage rules for plant-pollinator networks: trait complementarity or exploitation barriers? PLoS Biol. 5, e31 (2007)

    Article  Google Scholar 

  16. 16

    Guimarães, P. R. Jr, Jordano, P. & Thompson, J. N. Evolution and coevolution in mutualistic networks. Ecol. Lett. 14, 877–885 (2011)

    Article  Google Scholar 

  17. 17

    Elias, M., Gompert, Z., Jiggins, C. & Willmott, K. Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol. 6, 2642–2649 (2008)

    CAS  Article  Google Scholar 

  18. 18

    Fontaine, C. et al. The ecological and evolutionary implications of merging different types of networks. Ecol. Lett. 14, 1170–1181 (2011)

    Article  Google Scholar 

  19. 19

    Hastings, A. Transients: the key to long-term ecological understanding? Trends Ecol. Evol. 19, 39–45 (2004)

    Article  Google Scholar 

  20. 20

    Terborgh, T. & Estes, J. A. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature (Island, 2010)

  21. 21

    Levine, J. M., Bascompte, J., Adler, P. B. & Allesina, S. Beyond pairwise mechanisms of species coexistence in complex communities. Nature 546, 56–64 (2017)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Dyer, R. J. & Nason, J. D. Population graphs: the graph theoretic shape of genetic structure. Mol. Ecol. 13, 1713–1727 (2004)

    Article  Google Scholar 

  23. 23

    Haldane, A. G. & May, R. M. Systemic risk in banking ecosystems. Nature 469, 351–355 (2011)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Fowler, J. H. & Christakis, N. A. Cooperative behavior cascades in human social networks. Proc. Natl Acad. Sci. USA 107, 5334–5338 (2010)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Eriksson, O. Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biol. Rev. Camb. Philos. Soc. 91, 168–186 (2016)

    Article  Google Scholar 

  26. 26

    Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008)

    Article  Google Scholar 

  27. 27

    Miller-Struttmann, N. E. et al. Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349, 1541–1544 (2015)

    ADS  CAS  Article  Google Scholar 

  28. 28

    Marquitti, F. M. D., Guimarães, P. R., Pires, M. M. & Bittencourt, L. F. MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37, 221–224 (2014)

    Article  Google Scholar 

  29. 29

    Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Loyola, R. D. & Ulrich, W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239 (2008)

    Article  Google Scholar 

  30. 30

    Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant-animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003)

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

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).

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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.

Corresponding author

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). https://doi.org/10.1038/nature24273

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