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Coexistence holes characterize the assembly and disassembly of multispecies systems

Abstract

A central goal of ecological research has been to understand the limits on the maximum number of species that can coexist under given constraints. However, we know little about the assembly and disassembly processes under which a community can reach such a maximum number, or whether this number is in fact attainable in practice. This limitation is partly due to the challenge of performing experimental work and partly due to the lack of a formalism under which one can systematically study such processes. Here, we introduce a formalism based on algebraic topology and homology theory to study the space of species coexistence formed by a given pool of species. We show that this space is characterized by ubiquitous discontinuities that we call coexistence holes (that is, empty spaces surrounded by filled space). Using theoretical and experimental systems, we provide direct evidence showing that these coexistence holes do not occur arbitrarily—their diversity is constrained by the internal structure of species interactions and their frequency can be explained by the external factors acting on these systems. Our work suggests that the assembly and disassembly of ecological systems is a discontinuous process that tends to obey regularities.

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Fig. 1: Coexistence holes characterize discontinuities in assembly and disassembly processes.
Fig. 2: Assembly and disassembly holes in classic ecological models.
Fig. 3: Homology reveals the essential structure of assembly and disassembly hypergraphs in terms of their skeletons.
Fig. 4: A structuralist approach to understanding the emergence of coexistence holes in the Lotka–Volterra model.
Fig. 5: Assembly and disassembly holes in empirical ecological systems.

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Data availability

All of the data analysed in this study are publicly available.

Code availability

The code supporting the results is archived in the GitHub repository at https://syntheticdynamics.github.io/CoexistenceHoles.jl.

References

  1. Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).

    Article  Google Scholar 

  2. Tylianakis, J. M., Martínez-García, L. B., Richardson, S. J., Peltzer, D. A. & Dickie, I. A. Symmetric assembly and disassembly processes in an ecological network. Ecol. Lett. 21, 896–904 (2018).

    Article  PubMed  Google Scholar 

  3. Chase, J. M., Blowes, S. A., Knight, T. M., Gerstner, K. & May, F. Ecosystem decay exacerbates biodiversity loss with habitat loss. Nature 584, 238–243 (2020).

    Article  CAS  PubMed  Google Scholar 

  4. Vellend, M. The Theory of Ecological Communities (MPB-57) (Princeton Univ. Press, 2016).

  5. Hutchinson, G. E. Homage to Santa Rosalia or why are there so many kinds of animals? Am. Nat. 93, 145–159 (1959).

    Article  Google Scholar 

  6. Tilman, D. Resource Competition and Community Structure (Princeton Univ. Press, 1982).

  7. Barbier, M., Arnoldi, J.-F., Bunin, G. & Loreau, M. Generic assembly patterns in complex ecological communities. Proc. Natl Acad. Sci. USA 115, 2156–2161 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Serván, C. A., Capitán, J. A., Grilli, J., Morrison, K. E. & Allesina, S. Coexistence of many species in random ecosystems. Nat. Ecol. Evol. 2, 1237–1242 (2018).

    Article  PubMed  Google Scholar 

  9. MacArthur, R. Species packing and competitive equilibrium for many species. Theor. Popul. Biol. 1, 1–11 (1970).

    Article  CAS  PubMed  Google Scholar 

  10. Medeiros, L. P., Boege, K., del Val, E., Zaldivar-Riverón, A. & Saavedra, S. Observed ecological communities are formed by species combinations that are among the most likely to persist under changing environments. Am. Nat. https://doi.org/10.1086/711663 (2020).

  11. Barabás, G., D’Andrea, R. & Stump, S. M. Chesson’s coexistence theory. Ecol. Monogr. 88, 277–303 (2018).

    Article  Google Scholar 

  12. Grainger, T. N. & Gilbert, J. M. L. B. The invasion criterion: a common currency for ecological research. Trends Ecol. Evol. 34, 925–935 (2019).

    Article  PubMed  Google Scholar 

  13. Alberch, P. The logic of monsters: evidence for internal constraint in development and evolution. Geobios 22, 21–57 (1989).

    Article  Google Scholar 

  14. Clements, F. E. Nature and structure of the climax. J. Ecol. 24, 252–284 (1936).

    Article  Google Scholar 

  15. Odum, E. P. & Barrett, G. W. Fundamentals of Ecology 5th edn (Thomson Brooks/Cole, 2005).

  16. Friedman, J., Higgins, L. M. & Gore, J. Community structure follows simple assembly rules in microbial microcosms. Nat. Ecol. Evol. 1, 0109 (2017).

    Article  Google Scholar 

  17. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).

    Article  Google Scholar 

  18. Drake, J. A. Community-assembly mechanics and the structure of an experimental species ensemble. Am. Nat. 137, 1–26 (1991).

    Article  Google Scholar 

  19. Warren, P. H., Law, R. & Weatherby, A. J. Mapping the assembly of protist communities in microcosms. Ecology 84, 1001–1011 (2003).

    Article  Google Scholar 

  20. Schreiber, S. J. & Rittenhouse, S. From simple rules to cycling in community assembly. Oikos 105, 349–358 (2004).

    Article  Google Scholar 

  21. Chase, J. M. & Leibold, M. A. Ecological Niches: Linking Classical and Contemporary Approaches (Univ. Chicago Press, 2003).

  22. Kraft, N. J. et al. Community assembly, coexistence and the environmental filtering metaphor. Funct. Ecol. 29, 592–599 (2015).

    Article  Google Scholar 

  23. Moore, R., Robinson, W., Lovette, I. & Robinson, T. Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol. Lett. 11, 960–968 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. Maherali, H. & Klironomos, J. N. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316, 1746–1748 (2007).

    Article  CAS  PubMed  Google Scholar 

  25. Serván, C. & Allesina, S. Tractable models of ecological assembly. Ecol. Lett. 24, 1029–1037 (2021).

    Article  PubMed  Google Scholar 

  26. Rosindell, J., Hubbell, S. P. & Etienne, R. S. The unified neutral theory of biodiversity and biogeography at age ten. Trends Ecol. Evol. 26, 340–348 (2011).

    Article  PubMed  Google Scholar 

  27. Case, T. J. Surprising behavior from a familiar model and implications for competition theory. Am. Nat. 146, 961–966 (1995).

    Article  Google Scholar 

  28. Saavedra, S. et al. A structural approach for understanding multispecies coexistence. Ecol. Monogr. 87, 470–486 (2017).

    Article  Google Scholar 

  29. Tilman, D. Resources: a graphical-mechanistic approach to competition and predation. Am. Nat. 116, 362–393 (1980).

    Article  Google Scholar 

  30. May, R. M. & Leonard, W. J. Nonlinear aspects of competition between three species. SIAM J. Appl. Math. 29, 243–253 (1975).

    Article  Google Scholar 

  31. Dean, A. M. A simple model of mutualism. Am. Nat. 121, 409–417 (1983).

    Article  Google Scholar 

  32. Song, C., Ahn, S. V., Rohr, R. P. & Saavedra, S. Towards a probabilistic understanding about the context-dependency of species interactions. Trends Ecol. Evol. 35, 384–396 (2020).

    Article  PubMed  Google Scholar 

  33. Saavedra, S., Medeiros, L. P. & AlAdwani, M. Structural forecasting of species persistence under changing environments. Ecol. Lett. https://doi.org/10.1111/ele.13582 (2020).

  34. Law, R. & Blackford, J. C. Self-assembling food webs: a global viewpoint of coexistence of species in Lotka–Volterra communities. Ecology 73, 567–578 (1992).

    Article  Google Scholar 

  35. Sigmuiud, K. Darwin’s ‘circles of complexity’: assembling ecological communities. Complexity 1, 40–44 (1995).

    Article  Google Scholar 

  36. Law, R. & Morton, R. D. Permanence and the assembly of ecological communities. Ecology 77, 762–775 (1996).

    Article  Google Scholar 

  37. Wilson, J. B., Spijkerman, E. & Huisman, J. Is there really insufficient support for Tilman’s R* concept? A comment on Miller et al. Am. Nat. 169, 700–706 (2007).

    Article  PubMed  Google Scholar 

  38. May, R. M. Simple mathematical models with very complicated dynamics. Nature 261, 459–467 (1976).

    Article  CAS  PubMed  Google Scholar 

  39. Cenci, S., Song, C. & Saavedra, S. Rethinking the importance of the structure of ecological networks under an environment-dependent framework. Ecol. Evol. 8, 6852–6859 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  40. O’Dwyer, J. P. Whence Lotka-Volterra? Theor. Ecol. 11, 441–452 (2018).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  42. Vandermeer, J. H. The competitive structure of communities: an experimental approach with protozoa. Ecology 50, 362–371 (1969).

    Article  Google Scholar 

  43. Stein, R. R. et al. Ecological modeling from time-series inference: insight into dynamics and stability of intestinal microbiota. PLoS Comput. Biol. 9, e1003388 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Venturelli, O. S. et al. Deciphering microbial interactions in synthetic human gut microbiome communities. Mol. Syst. Biol. 14, e8157 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Bucci, V. et al. MDSINE: Microbial Dynamical Systems Inference Engine for microbiome time-series analyses. Genome Biol. 17, 121 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Turelli, M. A reexamination of stability in randomly varying versus deterministic environments with comments on the stochastic theory of limiting similarity. Theor. Popul. Biol. 13, 244–267 (1978).

    Article  CAS  PubMed  Google Scholar 

  47. May, R. M. Stability and Complexity in Model Ecosystems (Princeton Univ. Press, 2019).

  48. Allesina, S. & Tang, S. The stability–complexity relationship at age 40: a random matrix perspective. Popul. Ecol. 57, 63–75 (2015).

    Article  Google Scholar 

  49. Allesina, S. & Tang, S. Stability criteria for complex ecosystems. Nature 483, 205–208 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Grilli, J., Rogers, T. & Allesina, S. Modularity and stability in ecological communities. Nat. Commun. 7, 12031 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hoek, T. A. et al. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS Biol. 14, e1002540 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Case, T. J. An Illustrated Guide to Theoretical Ecology (Oxford Univ. Press, 2000).

  53. Freedman, H. & So, J.-H. Global stability and persistence of simple food chains. Math. Biosci. 76, 69–86 (1985).

    Article  Google Scholar 

  54. Posfai, A., Taillefumier, T. & Wingreen, N. S. Metabolic trade-offs promote diversity in a model ecosystem. Phys. Rev. Lett. 118, 028103 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl Acad. Sci. USA 115, E11951–E11960 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kehe, J. et al. Massively parallel screening of synthetic microbial communities. Proc. Natl Acad. Sci. USA 116, 12804–12809 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Xiao, Y. et al. Mapping the ecological networks of microbial communities. Nat. Commun. 8, 2042 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  58. AlAdwani, M. & Saavedra, S. Is the addition of higher-order interactions in ecological models increasing the understanding of ecological dynamics? Math. Biosci. 315, 108222 (2019).

    Article  PubMed  Google Scholar 

  59. Weibel, C. A. in History of Topology (ed. James, I.) 797–836 (North-Holland, 1999).

  60. Carlsson, G. Topology and data. Bull. Am. Math. Soc. 46, 255–308 (2009).

    Article  Google Scholar 

  61. Rabadán, R. & Blumberg, A. J. Topological Data Analysis for Genomics and Evolution: Topology in Biology (Cambridge Univ. Press, 2019).

  62. Sizemore, A. E., Phillips-Cremins, J. E., Ghrist, R. & Bassett, D. S. The importance of the whole: topological data analysis for the network neuroscientist. Netw. Neurosci. 3, 656–673 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Sugihara, G. Graph theory, homology and food webs. In Proc. Symposia in Applied Mathematics 30, 83–101 (American Mathematical Society, 1984).

  64. Singh, G., Mémoli, F. & Carlsson, G. E. Topological methods for the analysis of high dimensional data sets and 3D object recognition. In Symposium on Point Based Graphics 91–100 (The Eurographics Association, 2007).

  65. Giusti, C., Ghrist, R. & Bassett, D. S. Two’s company, three (or more) is a simplex. J. Comput. Neurosci. 41, 1–14 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Bauer, U. Ripser: efficient computation of Vietoris–Rips persistence barcodes. Preprint at https://arxiv.org/abs/1908.02518 (2019).

  67. Fort, H. On predicting species yields in multispecies communities: quantifying the accuracy of the linear Lotka–Volterra generalized model. Ecol. Model. 387, 154–162 (2018).

    Article  Google Scholar 

  68. Halty, V., Valdés, M., Tejera, M., Picasso, V. & Fort, H. Modeling plant interspecific interactions from experiments with perennial crop mixtures to predict optimal combinations. Ecol. Appl. 27, 2277–2289 (2017).

    Article  PubMed  Google Scholar 

  69. Tabi, A. et al. Species multidimensional effects explain idiosyncratic responses of communities to environmental change. Nat. Ecol. Evol. 4, 1036–1043 (2020).

    Article  PubMed  Google Scholar 

  70. Jansen, W. A permanence theorem for replicator and Lotka–Volterra systems. J. Math. Biol. 25, 411–422 (1987).

    Article  Google Scholar 

  71. Schreiber, S. J. Criteria for Cr robust permanence. J. Differ. Equ. 162, 400–426 (2000).

    Article  Google Scholar 

  72. Angulo, M. T., Moreno, J. A., Lippner, G., Barabási, A.-L. & Liu, Y.-Y. Fundamental limitations of network reconstruction from temporal data. J. R. Soc. Interface 14, 20160966 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We gratefully acknowledge financial support from CONACyT grant number A1-S-13909 (M.T.A.) and NSF grant number DEB-2024349 (S.S.).

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M.T.A. conceived of the idea of coexistence holes. M.T.A., C.S. and S.S. designed and realized the study. M.T.A., L.M. and A.K. performed the theoretical analysis. M.T.A., C.S. and S.S. wrote the manuscript. A.K. and M.T.A. wrote the software package to identify coexistence holes. All authors revised the manuscript.

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Correspondence to Marco Tulio Angulo or Serguei Saavedra.

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Peer review information Nature Ecology & Evolution thanks Stefano Allesina, Andrew Letten and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Angulo, M.T., Kelley, A., Montejano, L. et al. Coexistence holes characterize the assembly and disassembly of multispecies systems. Nat Ecol Evol 5, 1091–1101 (2021). https://doi.org/10.1038/s41559-021-01462-8

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