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Ecosystem tipping points in an evolving world

Abstract

There is growing concern over tipping points arising in ecosystems because of the crossing of environmental thresholds. Tipping points lead to abrupt and possibly irreversible shifts between alternative ecosystem states, potentially incurring high societal costs. Trait variation in populations is central to the biotic feedbacks that maintain alternative ecosystem states, as they govern the responses of populations to environmental change that could stabilize or destabilize ecosystem states. However, we know little about how evolutionary changes in trait distributions over time affect the occurrence of tipping points and even less about how big-scale ecological shifts reciprocally interact with trait dynamics. We argue that interactions between ecological and evolutionary processes should be taken into account in order to understand the balance of feedbacks governing tipping points in nature.

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References

  1. 1.

    Scheffer, M., Hosper, S. H., Meijer, M. L., Moss, B. & Jeppesen, E. Alternative equilibria in shallow lakes. Trends Ecol. Evol. 8, 275–279 (1993).

  2. 2.

    Reynolds, J. F. et al. Global desertification: building a science for dryland development. Science 316, 847–851 (2007).

  3. 3.

    Oliver, T. H. et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 30, 673–684 (2015).

  4. 4.

    Scheffer, M. Critical Transitions in Nature and Society. Princeton Studies in Complexity. (Princeton University Press, Princeton, NJ, USA, 2009).

  5. 5.

    Saccheri, I. & Hanski, I. Natural selection and population dynamics. Trends Ecol. Evol. 21, 341–347 (2006).

  6. 6.

    Kinnison, M. T. & Hairston, N. G. Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct. Ecol. 21, 444–454 (2007).

  7. 7.

    Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Jr. Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424, 303–306 (2003).

  8. 8.

    Pantel, J. H., Duvivier, C. & Meester, L. D. Rapid local adaptation mediates zooplankton community assembly in experimental mesocosms. Ecol. Lett. 18, 992–1000 (2015).

  9. 9.

    Farkas, T. E., Mononen, T., Comeault, A. A., Hanski, I. & Nosil, P. Evolution of camouflage drives rapid ecological change in an insect community. Curr. Biol. 23, 1835–1843 (2013).

  10. 10.

    Norberg, J. et al. Phenotypic diversity and ecosystem functioning in changing environments: a theoretical framework. Proc. Natl Acad. Sci. USA 98, 11376–11381 (2001).

  11. 11.

    Matthews, B. et al. Toward an integration of evolutionary biology and ecosystem science. Ecol. Lett. 14, 690–701 (2011).

  12. 12.

    Hendry, A. P. Eco-evolutionary Dynamics. (Princeton University Press, Princeton, NJ, USA, 2017).

  13. 13.

    De Mazancourt, C., Loreau, M. & Abbadie, L. Grazing optimization and nutrient cycling: When do herbivores enhance plant production? Ecology 79, 2242–2252 (1998).

  14. 14.

    Gravel, D. et al. Experimental niche evolution alters the strength of the diversity–productivity relationship. Nature 469, 89–92 (2011).

  15. 15.

    Loeuille, N., Loreau, M. & Ferrière, R. Consequences of plant–herbivore coevolution on the dynamics and functioning of ecosystems. J. Theor. Biol. 217, 369–381 (2002).

  16. 16.

    Boudsocq, S. et al. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am. Nat. 180, 60–69 (2012).

  17. 17.

    Anderson, C. N. K. et al. Why fishing magnifies fluctuations in fish abundance. Nature 452, 835–839 (2008).

  18. 18.

    Kuparinen, A., Boit, A., Valdovinos, F. S., Lassaux, H. & Martinez, N. D. Fishing-induced life-history changes degrade and destabilize harvested ecosystems. Sci. Rep. 6, 22245 (2016).

  19. 19.

    Hutchings, J. A. & Reynolds, J. D. Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54, 297–309 (2004).

  20. 20.

    Clements, C. F. & Ozgul, A. Including trait-based early warning signals helps predict population collapse. Nat. Commun. 7, 10984 (2016).

  21. 21.

    Clements, C. F. & Ozgul, A. Indicators of transitions in biological systems. Ecol. Lett. 21, 905–919 (2018).

  22. 22.

    Spanbauer, T. L. et al. Body size distributions signal a regime shift in a lake ecosystem. Proc. Biol. Sci. 283, 20160249 (2016).

  23. 23.

    Peterson, G., Allen, C. R. & Holling, C. S. Ecological resilience, biodiversity, and scale. Ecosystems (N. Y.) 1, 6–18 (1998).

  24. 24.

    Elmqvist, T. et al. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494 (2003).

  25. 25.

    Vellend, M. & Geber, M. A. Connections between species diversity and genetic diversity. Ecol. Lett. 8, 767–781 (2005).

  26. 26.

    Enquist, B.J. et al. Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theories. Adv. Ecol. Res. 52, 249–318 (2015).

  27. 27.

    Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. Camb. Philos. Soc. 88, 349–364 (2013).

  28. 28.

    Cortez, M. H. Comparing the qualitatively different effects rapidly evolving and rapidly induced defences have on predator-prey interactions. Ecol. Lett. 14, 202–209 (2011).

  29. 29.

    Hansen, M. M., Olivieri, I., Waller, D. M. & Nielsen, E. E. Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21, 1311–1329 (2012).

  30. 30.

    Nei, M. The new mutation theory of phenotypic evolution. Proc. Natl Acad. Sci. USA 104, 12235–12242 (2007).

  31. 31.

    Ortiz-Barrientos, D., Engelstädter, J. & Rieseberg, L. H. Recombination rate evolution and the origin of species. Trends Ecol. Evol. 31, 226–236 (2016).

  32. 32.

    Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).

  33. 33.

    Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011).

  34. 34.

    Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010).

  35. 35.

    Ruel, J. J. & Ayres, M. P. Jensen’s inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361–366 (1999).

  36. 36.

    Gomulkiewicz, R. & Holt, R. D. When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995).

  37. 37.

    Bell, G. & Gonzalez, A. Evolutionary rescue can prevent extinction following environmental change. Ecol. Lett. 12, 942–948 (2009).

  38. 38.

    Dieckmann, U. & Ferriere, R. in Evolutionary Conservation Biology (eds. Ferrière, R. & Ulf Dieckmann, D. C. B.) 188–224 (Cambridge University Press, Cambridge, 2004).

  39. 39.

    Rankin, D. J. & Lopez-Sepulcre, A. Can adaptation lead to extinction? Oikos 111, 616–619 (2005).

  40. 40.

    Gyllenberg, M. & Parvinen, K. Necessary and sufficient conditions for evolutionary suicide. Bull. Math. Biol. 63, 981–993 (2001).

  41. 41.

    Ferriere, R. & Legendre, S. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120081 (2013).

  42. 42.

    Walsh, M. R., Munch, S. B., Chiba, S. & Conover, D. O. Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecol. Lett. 9, 142–148 (2006).

  43. 43.

    Olsen, E. M. et al. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428, 932–935 (2004).

  44. 44.

    Kéfi, S., van Baalen, M., Rietkerk, M. & Loreau, M. Evolution of local facilitation in arid ecosystems. Am. Nat. 172, E1–E17 (2008).

  45. 45.

    Murray, G. G. R. et al. Natural selection shaped the rise and fall of passenger pigeon genomic diversity. Science 358, 951–954 (2017).

  46. 46.

    Faassen, E. J. et al. Hysteresis in an experimental phytoplankton population. Oikos 124, 1617–1623 (2015).

  47. 47.

    Abrams, P. A. ‘Adaptive Dynamics’ vs. ‘adaptive dynamics’. J. Evol. Biol. 18, 1162–1165 (2005).

  48. 48.

    Patel, S., Cortez, M. H. & Schreiber, S. J. Partitioning the effects of eco-evolutionary feedbacks on community stability. Am. Nat. 191, 1–29 (2016).

  49. 49.

    Fukami, T. & Morin, P. J. Productivity-biodiversity relationships depend on the history of community assembly. Nature 424, 423–426 (2003).

  50. 50.

    Dai, L., Vorselen, D., Korolev, K. S. & Gore, J. Generic indicators for loss of resilience before a tipping point leading to population collapse. Science 336, 1175–1177 (2012).

  51. 51.

    Veraart, A. J. A. J. et al. Recovery rates reflect distance to a tipping point in a living system. Nature 481, 357–359 (2011).

  52. 52.

    Sirota, J., Baiser, B., Gotelli, N. J. & Ellison, A. M. Organic-matter loading determines regime shifts and alternative states in an aquatic ecosystem. Proc. Natl Acad. Sci. USA 110, 7742–7747 (2013).

  53. 53.

    Lau, M. K., Baiser, B., Northrop, A., Gotelli, N. J. & Ellison, A. M. Regime shifts and hysteresis in the pitcher-plant microecosystem. Ecol. Modell. 382, 1–8 (2018).

  54. 54.

    Becks, L., Ellner, S. P., Jones, L. E. & Hairston, N. G. Jr. Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. Ecol. Lett. 13, 989–997 (2010).

  55. 55.

    Williams, J. L., Kendall, B. E. & Levine, J. M. Rapid evolution accelerates plant population spread in fragmented experimental landscapes. Science 353, 482–485 (2016).

  56. 56.

    Franklin, O. D. & Morrissey, M. B. Inference of selection gradients using performance measures as fitness proxies. Methods Ecol. Evol. 8, 663–677 (2017).

  57. 57.

    Pimentel, D. Population regulation and genetic feedback. Science 159, 1432–1437 (1968).

  58. 58.

    Levins, R. Evolution In Changing Environments: Some Theoretical Explorations. Monographs in Population Biology. (Princeton University Press, Princeton, NJ, USA, 1968).

  59. 59.

    Fussmann, G. F., Loreau, M. & Abrams, Pa Eco-evolutionary dynamics of communities and ecosystems. Funct. Ecol. 21, 465–477 (2007).

  60. 60.

    Matthews, B. et al. Under niche construction: an operational bridge between ecology, evolution, and ecosystem science. Ecol. Monogr. 84, 245–263 (2015).

  61. 61.

    Dercole, F., Ferrière, R. & Rinaldi, S. Ecological bistability and evolutionary reversals under asymmetrical competition. Evolution 56, 1081–1090 (2002).

  62. 62.

    Driscoll, W. W., Hackett, J. D. & Ferrière, R. Eco-evolutionary feedbacks between private and public goods: evidence from toxic algal blooms. Ecol. Lett. 19, 81–97 (2016).

  63. 63.

    DeLong, J. P. et al. How fast is fast? Eco-evolutionary dynamics and rates of change in populations and phenotypes. Ecol. Evol. 6, 573–581 (2016).

  64. 64.

    terHorst, C. P. et al. evolution in a community context: trait responses to multiple species interactions. Am. Nat. 191, https://doi.org/10.1086/695835 (2018).

  65. 65.

    Carpenter, S. R. et al. Early warnings of regime shifts: a whole-ecosystem experiment. Science 332, 1079–1082 (2011).

  66. 66.

    Van Dijk, G. M. & Van Vierssen, W. Survival of a Potamogeton pectinatus L. population under various light conditions in a shallow eutrophic lake Lake Veluwe in The Netherlands. Aquat. Bot. 39, 121–130 (1991).

  67. 67.

    Hilt, S. et al. Response of submerged macrophyte communities to external and internal restoration measures in north temperate shallow lakes. Front. Plant Sci. 9, 194 (2018).

  68. 68.

    Van Donk, E., Gulati, R. D., Iedema, A. & Meulemans, J. T. Macrophyte-related shifts in the nitrogen and phosphorus contents of the different trophic levels in a biomanipulated shallow lake. Hydrobiologia 251, 19–26 (1993).

  69. 69.

    Madsen, T. V. & Cedergreen, N. Sources of nutrients to rooted submerged macrophytes growing in a nutrient-rich stream. Freshw. Biol. 47, 283–291 (2002).

  70. 70.

    Ibelings, B. W. et al. Resilience of alternative stable states during the recovery of shallow lakes from eutrophication: Lake Veluwe as a case study. Ecosystems 10, 4–16 (2007).

  71. 71.

    Milchunas, D. G. & Noy-Meir, I. Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99, 113–130 (2002).

  72. 72.

    Rietkerk, M. et al. Self-organization of vegetation in arid ecosystems. Am. Nat. 160, 524–530 (2002).

  73. 73.

    Archer, S. R. & Scholes, R. Tree–grass interactions. Annu. Rev. Ecol. Syst. 28, 527–544 (1997).

  74. 74.

    Staver, A. C., Archibald, S. & Levin, S. A. The global extent and determinants of savanna and forest as alternative biome states. Science 334, 230–232 (2011).

  75. 75.

    Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003).

  76. 76.

    Mumby, P. J. & Steneck, R. S. Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol. Evol. 23, 555–563 (2008).

  77. 77.

    van Belzen, J. et al. Vegetation recovery in tidal marshes reveals critical slowing down under increased inundation. Nat. Commun. 8, 15811 (2017).

  78. 78.

    Bouma, T. J. et al. Short-term mudflat dynamics drive long-term cyclic salt marsh dynamics. Limnol. Oceanogr. 61, 2261–2275 (2016).

  79. 79.

    Maxwell, P. S. et al. The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems - a review. Biol. Rev. Camb. Philos. Soc. 92, 1521–1538 (2017).

  80. 80.

    Williams, N. M. et al. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 143, 2280–2291 (2010).

  81. 81.

    Lever, J. J., van Nes, E. H., Scheffer, M. & Bascompte, J. The sudden collapse of pollinator communities. Ecol. Lett. 17, 350–359 (2014).

  82. 82.

    Filbee-Dexter, K. & Scheibling, R. Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar. Ecol. Prog. Ser. 495, 1–25 (2013).

  83. 83.

    van Nes, E. H. et al. What do you mean, ‘tipping point’? Trends Ecol. Evol. 31, 902–904 (2016).

  84. 84.

    Strogatz, S.H. Nonlinear Dynamics and Chaos with Applications to Physics, Biology, Chemistry and Engineering. (Perseus Books, 1994).

  85. 85.

    Petraitis, P. S., Methratta, E. T., Rhile, E. C., Vidargas, N. A. & Dudgeon, S. R. Experimental confirmation of multiple community states in a marine ecosystem. Oecologia 161, 139–148 (2009).

  86. 86.

    Barnosky, A. D. et al. Approaching a state shift in Earth’s biosphere. Nature 486, 52–58 (2012).

  87. 87.

    Knowlton, N. Thresholds and multiple stable states in coral reef community dynamics. Am. Zool. 32, 674–682 (1992).

  88. 88.

    Beddington, J. R. & May, R. M. Harvesting natural populations in a randomly fluctuating environment. Science 197, 463–465 (1977).

  89. 89.

    Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).

  90. 90.

    Dakos, V., Carpenter, S. R., Van Nes, E. H. & Scheffer, M. Resilience indicators: prospects and limitations for early warnings of regime shifts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20130263 (2015).

  91. 91.

    Baruah, G., Clements, C.F., Guillaume, F. & Ozgul, A. When do shifts in trait dynamics precede population declines? Preprint at https://doi.org/10.1101/424671 (2018).

  92. 92.

    Osmond, M. M. & Klausmeier, C. A. An evolutionary tipping point in a changing environment. Evolution 71, 2930–2941 (2017).

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Acknowledgements

The authors thank C. Clements and G. Baruah for their helpful comments. V.D. and B.M. are grateful to Eawag and the Adaptation to a Changing Environment Program at ETH Zurich for financing a workshop on eco-evolutionary dynamics of tipping points held in Kastanienbaum in 2016. B.M. acknowledges a SNF 31003A_175614 grant.

Author information

V.D. and B.M. designed the research and wrote the paper, with contributions from all authors.

Competing interests

The authors declare no competing interests.

Correspondence to Vasilis Dakos or Blake Matthews.

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Fig. 1: Variation in a response trait (such as macrophyte shading tolerance) affects the tipping point at which a shallow lake shifts to a eutrophic turbid state.
Fig. 2: Hypothetical alterations of trajectories of ecosystem collapse (left panels, red solid lines) as a consequence of trait change (right panels, red dashed lines).
Fig. 3: Potential consequences of trait change on the recovery trajectories of an ecosystem after collapse.