Diversity begets diversity in competition for space

Abstract

Competition can profoundly affect biodiversity patterns by determining whether similar species are likely to coexist. When species compete directly for space, competitive ability differences should theoretically promote trait and phylogenetic clustering, provided that niche differences are otherwise minimal. Yet many sessile communities exhibit high biodiversity despite minimal reliance on niche differentiation. A potential explanation is that intransitive competition (‘rock–paper–scissors’ competition) not only promotes species richness but also fosters coexistence among highly dissimilar species with different competitive strategies. Here, we test this hypothesis using a combination of empirical and analytical approaches. In an experimental system comprising 37 wood-decay basidiomycete fungi grown in nutrient-rich agar media, pairwise displacement was maximized when species had widely different competitive traits and divergent evolutionary histories. However, when these interactions were embedded in models of species-rich communities, high levels of intransitivity ultimately overwhelmed the pairwise relationships, allowing the weakest and most dissimilar species to survive. In line with theoretical expectations, these multispecies assemblages exhibited reduced functional and phylogenetic diversity, yet the smallest losses were likewise observed in species-rich communities. By demonstrating that species richness can act as a self-reinforcing buffer against competitive exclusion, these results contribute to our understanding of how biodiversity is maintained in natural systems.

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Figure 1: The 23 fungal species used in the pairwise competition experiments.
Figure 2: Pairwise competitive exclusion was most likely when species were functionally and phylogenetically dissimilar.
Figure 3: Patch-occupancy model results linking community characteristics to losses in species richness.
Figure 4: Relationships between species richness and losses in phylogenetic dissimilarity and functional dissimilarity.

References

  1. 1

    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001).

    Google Scholar 

  2. 2

    Kraft, N. J. B., Godoy, O. & Levine, J. M. Plant functional traits and the multidimensional nature of species coexistence. Proc. Natl Acad. Sci. USA 112, 797–802 (2015).

    CAS  PubMed  Google Scholar 

  3. 3

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

    Google Scholar 

  4. 4

    Tokeshi, M. Species Coexistence: Ecological and Evolutionary Perspectives (Wiley, 1999).

  5. 5

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

    Google Scholar 

  6. 6

    Johnson, C. R. & Seinen, I. Selection for restraint in competitive ability in spatial competition systems. Proc. R. Soc. B 269, 655–663 (2002).

    PubMed  Google Scholar 

  7. 7

    Molofsky, J. & Bever, J. D. A novel theory to explain species diversity in landscapes: positive frequency dependence and habitat suitability. Proc. R. Soc. B 269, 2389–2393 (2002).

    PubMed  Google Scholar 

  8. 8

    Amarasekare, P. Interference competition and species coexistence. Proc. R. Soc. B 269, 2541–2550 (2002).

    PubMed  Google Scholar 

  9. 9

    Buss, A. L. W. & Jackson, J. B. C. Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat. 113, 223–234 (1979).

    Google Scholar 

  10. 10

    Laird, R. A. & Schamp, B. S. Competitive intransitivity promotes species coexistence. Am. Nat. 168, 182–193 (2006).

    PubMed  Google Scholar 

  11. 11

    Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. M. Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171–174 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Reichenbach, T., Mobilia, M. & Frey, E. Mobility promotes and jeopardizes biodiversity in rock–paper–scissors games. Nature 448, 1046–1049 (2007).

    CAS  PubMed  Google Scholar 

  13. 13

    Kirkup, B. C. & Riley, M. a. Antibiotic-mediated antagonism leads to a bacterial game of rock–paper–scissors in vivo . Nature 428, 412–414 (2004).

    CAS  PubMed  Google Scholar 

  14. 14

    Violle, C., Nemergut, D. R., Pu, Z. & Jiang, L. Phylogenetic limiting similarity and competitive exclusion. Ecol. Lett. 14, 782–787 (2011).

    PubMed  Google Scholar 

  15. 15

    Macarthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).

    Google Scholar 

  16. 16

    Mayfield, M. M. & Levine, J. M. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol. Lett. 13, 1085–1093 (2010).

    PubMed  Google Scholar 

  17. 17

    HilleRisLambers, J., Adler, P. B., Harpole, W. S., Levine, J. M. & Mayfield, M. M. Rethinking community assembly through the lens of coexistence theory. Annu. Rev. Ecol. Evol. Syst. 43, 227–248 (2012).

    Google Scholar 

  18. 18

    Chu, C. & Adler, P. B. Large niche differences emerge at the recruitment stage to stabilize grassland coexistence. Ecol. Monogr. 85, 373– 392 (2015).

    Google Scholar 

  19. 19

    Kunstler, G. et al. Competitive interactions between forest trees are driven by species’ trait hierarchy, not phylogenetic or functional similarity: implications for forest community assembly. Ecol. Lett. 15, 831–840 (2012).

    PubMed  PubMed Central  Google Scholar 

  20. 20

    Hardin, G. The competitive exclusion principle. Science 131, 1292–1297 (1960).

    CAS  PubMed  Google Scholar 

  21. 21

    Allesina, S. & Levine, J. M. A competitive network theory of species diversity. Proc. Natl Acad. Sci. USA 108, 5638–5642 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Jessup, C. M. et al. Big questions, small worlds: microbial model systems in ecology. Trends Ecol. Evol. 19, 189–197 (2004).

    PubMed  Google Scholar 

  23. 23

    Nahum, J. R., Harding, B. N. & Kerr, B. Evolution of restraint in a structured rock–paper–scissors community. Proc. Natl Acad. Sci. USA 108, 10831–10838 (2011).

    CAS  PubMed  Google Scholar 

  24. 24

    Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Boddy, L. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol. 31, 185–194 (2000).

    CAS  PubMed  Google Scholar 

  26. 26

    Navas, M.-L. & Violle, C. Plant traits related to competition: how do they shape the functional diversity of communities? Community Ecol. 10, 131–137 (2009).

    Google Scholar 

  27. 27

    Crowther, T. W. et al. Untangling the fungal niche: the trait-based approach. Front. Microbiol. 5, 579 (2014).

    PubMed  PubMed Central  Google Scholar 

  28. 28

    El Ariebi, N., Hiscox, J., Scriven, S. A., Müller, C. T. & Boddy, L. Production and effects of volatile organic compounds during interspecific interactions. Fungal Ecol. 20, 144–154 (2016).

    Google Scholar 

  29. 29

    Hiscox, J., Baldrian, P., Rogers, H. J. & Boddy, L. Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor . Fungal Genet. Biol. 47, 562–571 (2010).

    CAS  PubMed  Google Scholar 

  30. 30

    Maynard, D. S. et al. Modelling the multidimensional niche by linking functional traits to competitive performance. Proc. R. Soc. B 282, 20150516 (2015).

    Google Scholar 

  31. 31

    Amarasekare, P. Competitive coexistence in spatially structured environments: a synthesis. Ecol. Lett. 6, 1109–1122 (2003).

    Google Scholar 

  32. 32

    Ulrich, W., Soliveres, S., Kryszewski, W., Maestre, F. T. & Gotelli, N. J. Matrix models for quantifying competitive intransitivity from species abundance data. Oikos 123, 1057–1070 (2014).

    PubMed  PubMed Central  Google Scholar 

  33. 33

    Kunstler, G. et al. Plant functional traits have globally consistent effects on competition. Nature 529, 1–15 (2016).

    Google Scholar 

  34. 34

    Soliveres, S. et al. Intransitive competition is widespread in plant communities and maintains their species richness. Ecol. Lett. 18, 790–798 (2015).

    PubMed  PubMed Central  Google Scholar 

  35. 35

    Agren, G. I. & Fagerstrom, T. Limiting dissimilarity in plants: randomness prevents exclusion of species with similar competitive abilities. Oikos 43, 369–375 (1984).

    Google Scholar 

  36. 36

    Bastolla, U. et al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020 (2009).

    CAS  PubMed  Google Scholar 

  37. 37

    Alcántara, J. M., Pulgar, M. & Rey, P. J. Dissecting the role of transitivity and intransitivity on coexistence in competing species networks. Theor. Ecol. http://dx.doi.org/10.1007/s12080-016-0323-y (2016).

  38. 38

    Gallien, L. Intransitive competition and its effects on community functional diversity. Oikos 126, 615–623 (2016).

    Google Scholar 

  39. 39

    Treseder, K. K. et al. Evolutionary histories of soil fungi are reflected in their large-scale biogeography. Ecol. Lett. 17, 1086–1093 (2014).

    PubMed  Google Scholar 

  40. 40

    Godoy, O., Kraft, N. J. B. & Levine, J. M. Phylogenetic relatedness and the determinants of competitive outcomes. Ecol. Lett. 17, 836–844 (2014).

    PubMed  Google Scholar 

  41. 41

    Jackson, J. B. C. & Buss, L. Alleopathy and spatial competition among coral reef invertebrates. Proc. Natl Acad. Sci. USA 72, 5160–5163 (1975).

    CAS  PubMed  Google Scholar 

  42. 42

    Huisman, J., Johansson, A. M., Folmer, E. O. & Weissing, F. J. Towards a solution of the plankton paradox: the importance of physiology and life history. Ecol. Lett. 4, 408–411 (2001).

    Google Scholar 

  43. 43

    Huisman, J. & Weissing, F. J. Biodiversity of plankton by species oscillations and chaos. Nature 402, 407–410 (1999).

    Google Scholar 

  44. 44

    Vance, R. R. The stable coexistence of two competitors for one resource. Am. Nat. 126, 78–86 (1985).

    Google Scholar 

  45. 45

    Vance, R. R. Interference competition and the coexistence of two competitors on a single limiting resource. Ecology 65, 1349–1357 (1984).

    Google Scholar 

  46. 46

    Tilman, D. Competition and biodiversity in spatially structured habitats. Ecology 75, 2–16 (1994).

    Google Scholar 

  47. 47

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

    Google Scholar 

  48. 48

    Billick, I. & Case, T. J. Higher order interactions in ecological communities: what are they and how can they be detected? Ecology 75, 1529–1543 (1994).

    Google Scholar 

  49. 49

    Abrams, P. A. Arguments in favor of higher-order interactions. Am. Nat. 121, 887–891 (1983).

    Google Scholar 

  50. 50

    Bairey, E ., Kelsic, E. D & Kishony, R. High-order species interactions shape ecosystem diversity. Nat. Commun. 7, 12285 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Brazee, N. J & Lindner, D. L. Unravelling the Phellinus pini s.l. complex in North America: A multilocus phylogeny and differentiation analysis of Porodaedalea. For. Pathol. 43, 132–143 (2013).

    Google Scholar 

  52. 52

    Crowther, T. W ., Boddy, L & Jones, T. H. Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167, 535–545 (2011).

    PubMed  Google Scholar 

  53. 53

    Crowther, T. W., Boddy, L. & Jones, T. H. Outcomes of fungal interactions are determined by soil invertebrate grazers. Ecol. Lett. 14, 1134–1142 (2011).

    PubMed  Google Scholar 

  54. 54

    Ritchie, F ., McQuilken, M. P & Bain, R. A. Effects of water potential on mycelial growth, sclerotial production, and germination of Rhizoctonia solani from potato. Mycol. Res. 110, 725–733 (2006).

    PubMed  Google Scholar 

  55. 55

    Nesci, A., Etcheverry, M. & Magan, N. Osmotic and matric potential effects on growth, sugar alcohol and sugar accumulation by Aspergillus section Flavi strains from Argentina. J. Appl. Microbiol. 96, 965–972 (2004).

    CAS  PubMed  Google Scholar 

  56. 56

    Baldrian, P. et al. Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338, 111–125 (2010).

    Google Scholar 

  57. 57

    Žifčáková, L., Dobiášová, P., Kolářová, Z., Koukol, O. & Baldrian, P. Enzyme activities of fungi associated with Picea abies needles. Fungal Ecol. 4, 427–436 (2011).

    Google Scholar 

  58. 58

    Crowther, T. W. et al. Biotic interactions mediate soil microbial feedbacks to climate change. Proc. Natl Acad. Sci. USA 112, 7033–7038 (2015).

    CAS  PubMed  Google Scholar 

  59. 59

    Magan, N. & Lacey, J. Effect of water activity, temperature and substrate on interactions between field and storage fungi. Trans. Br. Mycol. Soc. 82, 83–93 (1984).

    Google Scholar 

  60. 60

    Evans, J. A., Eyre, C. A., Rogers, H. J., Boddy, L. & Müller, C. T. Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media. Fungal Ecol. 1, 57–68 (2008).

    Google Scholar 

  61. 61

    Rao, C. R. Diversity and dissimilarity coefficients: a unified approach. Theor. Popul. Biol. 21, 24–43 (1982).

    Google Scholar 

  62. 62

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  63. 63

    Ortiz-Santana, B., Lindner, D. L., Miettinen, O., Justo, A. & Hibbett, D. S. A phylogenetic overview of the antrodia clade (Basidiomycota, Polyporales). Mycologia 105, 1391–1411 (2013).

    CAS  PubMed  Google Scholar 

  64. 64

    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65

    Nei, M. & Kumar, S. Molecular Evolution and Phylogenetics (Oxford Univ. Press, 2000).

    Google Scholar 

  66. 66

    Felsentein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985).

    Google Scholar 

  67. 67

    Gascuel, O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14, 685–695 (1997).

    CAS  PubMed  Google Scholar 

  68. 68

    Tamura, K. et al. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69

    Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    PubMed  Google Scholar 

  70. 70

    Paradis, E. & Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Google Scholar 

  71. 71

    Kim, J. & Sanderson, M. J. Penalized likelihood phylogenetic inference: bridging the parsimony-likelihood gap. Syst. Biol 57, 665–674 (2008).

    PubMed  Google Scholar 

  72. 72

    Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol 19, 101–109 (2002).

    CAS  PubMed  Google Scholar 

  73. 73

    Cadotte, M. W. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc. Natl Acad. Sci. USA 110, 8996–9000 (2013).

    CAS  PubMed  Google Scholar 

  74. 74

    Liu, J. et al. Explaining maximum variation in productivity requires phylogenetic diversity and single functional traits. Ecology 96, 140702164956006 (2015).

    Google Scholar 

  75. 75

    Cadotte, M. W. & Davies, T. J. Phylogenies in Ecology: A Guide to Concepts and Methods (Princeton Univ. Press, 2016).

    Google Scholar 

  76. 76

    Sokal, R. & Michener, C. A statistical method for evaluating systematic relationships. Univ. Kansas Sci. Bull. 38, 1409–1438 (1958).

    Google Scholar 

  77. 77

    Elo, A. The Rating of Chess Players, Past and Present (Arco, 1987).

    Google Scholar 

  78. 78

    Horn, H. in Ecology and Evolution of Communities (eds Cody, M. & Diamond, J. ) 196–211 (Harvard Univ. Press, 1975).

    Google Scholar 

  79. 79

    Crowley, P. H. et al. A general model of local competition for space. Ecol. Lett. 8, 176–188 (2004).

    Google Scholar 

  80. 80

    Edwards, K. F. & Schreiber, S. J. Preemption of space can lead to intransitive coexistence of competitors. Oikos 119, 1201–1209 (2010).

    Google Scholar 

  81. 81

    Ódor, P. et al. Diversity of dead wood inhabiting fungi and bryophytes in semi-natural beech forests in Europe. Biol. Conserv. 131, 58–71 (2006).

    Google Scholar 

  82. 82

    Lindblad, I. Wood-inhabiting fungi on fallen logs of Norway spruce: relations to forest management and substrate quality. Nord. J. Bot. 18, 243–255 (1998).

    Google Scholar 

  83. 83

    Cooke, R. & Rayner, A. Ecology of Saprotrophic Fungi (Longman, 1984).

    Google Scholar 

  84. 84

    Petraitis, P. S. Competitive networks and measures of intransivity. Am. Nat. 114, 921–925 (1979).

    Google Scholar 

  85. 85

    Mouchet, M. A., Villéger, S., Mason, N. W. H. & Mouillot, D. Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct. Ecol. 24, 867–876 (2010).

    Google Scholar 

  86. 86

    Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002).

    Google Scholar 

  87. 87

    Clarke, K. & Warwick, R. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35, 523–531 (1998).

    Google Scholar 

  88. 88

    de Bello, F., Carmona, C. P., Lepš, J., Szava-Kovats, R. & Pärtel, M. Functional diversity through the mean trait dissimilarity: resolving shortcomings with existing paradigms and algorithms. Oecologia 180, 933–940 (2016).

    PubMed  Google Scholar 

  89. 89

    Helmus, M. R ., Bland, T. J ., Williams, C. K & Ives, A. R. Phylogenetic measures of biodiversity. Am. Nat. 169, E68–E83 (2007).

    PubMed  Google Scholar 

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Acknowledgements

We thank J. Levine and S. Allesina for their comments and discussions on earlier versions of this manuscript, and O. Schmitz, S. Kuebbing, S. Wood and C. Aguilar for their input on initial drafts. We also thank M. Peters for her assistance in the laboratory. This study was partially funded by the Yale Institute for Biospheric Studies (to D.S.M.), the Yale Climate and Energy Institute (to T.W.C), the British Ecological Society (to T.W.C.), the Marie Skłodowska-Curie Actions Fellowship (to T.W.C.), the US National Science Foundation (to M.A.B., T.W.C. and D.S.M., DEB-1601036, DEB-1021098 and DEB-1457614) and the US Forest Service.

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D.S.M. conceived the study, collected and analysed the data, and prepared the manuscript. T.W.C. and M.A.B. contributed equally to the study; T.W.C. helped to design the experiments, collect data and assist with manuscript preparation; M.A.B. assisted with the study design, conceptual advances and manuscript preparation; L.T.A.v.D. and S.D.F. performed enzyme analyses and supplied analytical tools; J.A.G. and D.L.L. provided fungal cultures, collected fungal trait data, and conducted DNA and phylogenetic analyses. All authors discussed the results and commented on the manuscript.

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Correspondence to Daniel S. Maynard.

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Maynard, D., Bradford, M., Lindner, D. et al. Diversity begets diversity in competition for space. Nat Ecol Evol 1, 0156 (2017). https://doi.org/10.1038/s41559-017-0156

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