Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1
Fig. 2
Fig. 3

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).

    CAS  PubMed  Google Scholar 

  2. 2.

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

    CAS  PubMed  Google Scholar 

  3. 3.

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

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  11. 11.

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

    PubMed  Google Scholar 

  12. 12.

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

    Google Scholar 

  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).

    Google Scholar 

  14. 14.

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

    CAS  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  16. 16.

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

    CAS  PubMed  Google Scholar 

  17. 17.

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

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

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

    Google Scholar 

  20. 20.

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

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

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

    PubMed  Google Scholar 

  22. 22.

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

    PubMed  PubMed Central  Google Scholar 

  23. 23.

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

    Google Scholar 

  24. 24.

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

    Google Scholar 

  25. 25.

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

    Google Scholar 

  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).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  30. 30.

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

    CAS  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  32. 32.

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

    Google Scholar 

  33. 33.

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

    PubMed  PubMed Central  Google Scholar 

  34. 34.

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

    CAS  PubMed  Google Scholar 

  35. 35.

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

    CAS  PubMed  Google Scholar 

  36. 36.

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

    PubMed  Google Scholar 

  37. 37.

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

    PubMed  Google Scholar 

  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).

    Google Scholar 

  40. 40.

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

    CAS  PubMed  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  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).

    PubMed  Google Scholar 

  43. 43.

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

    CAS  PubMed  Google Scholar 

  44. 44.

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

    PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  46. 46.

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

    Google Scholar 

  47. 47.

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

    CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  49. 49.

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

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  57. 57.

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

    CAS  PubMed  Google Scholar 

  58. 58.

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

    Google Scholar 

  59. 59.

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

    Google Scholar 

  60. 60.

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

    Google Scholar 

  61. 61.

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

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  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).

    Google Scholar 

  65. 65.

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

    CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  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).

    Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  Google Scholar 

  71. 71.

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

    Google Scholar 

  72. 72.

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

    PubMed  Google Scholar 

  73. 73.

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

    Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  75. 75.

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

    CAS  PubMed  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  77. 77.

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

    PubMed  PubMed Central  Google Scholar 

  78. 78.

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

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Google Scholar 

  83. 83.

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

    PubMed  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  86. 86.

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

    CAS  PubMed  Google Scholar 

  87. 87.

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

    Google Scholar 

  88. 88.

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

    CAS  PubMed  Google Scholar 

  89. 89.

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

    CAS  Google Scholar 

  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).

    PubMed Central  Google Scholar 

  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).

    PubMed  Google Scholar 

Download references

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

Affiliations

Authors

Contributions

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

Corresponding authors

Correspondence to Vasilis Dakos or Blake Matthews.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Information and Supplementary Figure 1

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dakos, V., Matthews, B., Hendry, A.P. et al. Ecosystem tipping points in an evolving world. Nat Ecol Evol 3, 355–362 (2019). https://doi.org/10.1038/s41559-019-0797-2

Download citation

Further reading

Search

Quick links