Skip to main content

Thank you for visiting 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.

Reconciling taxon senescence with the Red Queen’s hypothesis


In the fossil record, taxa exhibit a regular pattern of waxing and waning of occupancy, range or diversity between their origin and extinction. This pattern appears to contradict the law of constant extinction1, which states that the probability of extinction in a given taxon is independent of that taxon’s age. It is nevertheless well established for species, genera and higher taxa of terrestrial mammals2,3,4, marine invertebrates5,6,7, marine microorganisms8, and recent Hawaiian clades of animals and plants9. Here we show that the apparent contradiction between a stochastically constant extinction rate and the seemingly deterministic waxing and waning pattern of taxa disappears when we consider their peak of expansion rather than their final extinction. To a first approximation, we find that biotic drivers of evolution pertain mainly to the peak of taxon expansion, whereas abiotic drivers mainly apply to taxon extinction. The Red Queen’s hypothesis1, which emphasizes biotic interactions, was originally proposed as an explanation of the law of constant extinction. Much effort has since been devoted to determining how this hypothesis, emphasizing competition for resources, relates to the effects of environmental change. One proposed resolution is that biotic and abiotic processes operate at different scales10. By focusing attention on taxon expansion rather than survival, we resolve an apparent contradiction between the seemingly deterministic waxing and waning patterns over time and the randomness of extinction that the Red Queen’s hypothesis implies.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: The hat-like pattern of a taxon’s history in the fossil record.
Figure 2: Variations in patterns of population size over time with a range of random walk models.
Figure 3: Conceptual representation of the relationship between a taxon’s history and evolutionary drivers.


  1. Van Valen, L. A new evolutionary law. Evol. Theory 1, 1–30 (1973)

    Google Scholar 

  2. Jernvall, J. & Fortelius, M. Maintenance of trophic structure in fossil mammal communities: site occupancy and taxon resilience. Am. Nat. 164, 614–624 (2004)

    Article  Google Scholar 

  3. Quental, T. B. & Marshall, C. R. How the Red Queen drives terrestrial mammals to extinction. Science 341, 290–292 (2013)

    Article  CAS  ADS  Google Scholar 

  4. Carotenuto, F., Barbera, C. & Raia, P. Occupancy, range size, and phylogeny in Eurasian Pliocene to recent large mammals. Paleobiology 36, 399–414 (2010)

    Article  Google Scholar 

  5. Foote, M. et al. Rise and fall of species occupancy in Cenozoic fossil mollusks. Science 318, 1131–1134 (2007)

    Article  CAS  ADS  Google Scholar 

  6. Tietje, M. & Kiessling, W. Predicting extinction from fossil trajectories of geographical ranges in benthic marine molluscs. J. Biogeogr. 40, 790–799 (2013)

    Article  Google Scholar 

  7. Raia, P. et al. Progress to extinction: increased specialisation causes the demise of animal clades. Sci. Rep. 6, 30965 (2016)

    Article  CAS  ADS  Google Scholar 

  8. Liow, L. H. & Stenseth, N. C. The rise and fall of species: implications for macroevolutionary and macroecological studies. Proc. R. Soc. Lond. B 274, 2745–2752 (2007)

    Article  Google Scholar 

  9. Lim, J. Y. & Marshall, C. R. The true tempo of evolutionary radiation and decline revealed on the Hawaiian archipelago. Nature 543, 710–713 (2017)

    Article  CAS  ADS  Google Scholar 

  10. Barnosky, A. D. Distinguishing the effects of the Red Queen and Court Jester on Miocene mammal evolution in the northern Rocky Mountains. J. Vertebr. Paleontol. 21, 172–185 (2001)

    Article  Google Scholar 

  11. Marshall, C. R. Five palaeobiological laws needed to understand the evolution of the living biota. Nat. Ecol. Evol. 1, 0165 (2017)

    Article  Google Scholar 

  12. Van Valen, L. Energy and evolution. Evol. Theory 1, 179–229 (1976)

    Google Scholar 

  13. Van Valen, L. Evolution as a zero-sum game for energy. Evol. Theory 4, 289–300 (1980)

    Google Scholar 

  14. Rannikko, J., Žliobaite˙, I. & Fortelius, M. Relative abundances and palaeoecology of four suid genera in the Turkana Basin, Kenya, during the late Miocene to Pleistocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 487, 187–193 (2017)

    Article  Google Scholar 

  15. Raup, D. M., Gould, S. J., Schopf, T. J. M. & Simberloff, D. S. Stochastic models of phylogeny and the evolution of diversity. J. Geol. 81, 525–542 (1973)

    Article  ADS  Google Scholar 

  16. Cornette, J. L. & Lieberman, B. S. Random walks in the history of life. Proc. Natl Acad. Sci. USA 101, 187–191 (2004)

    Article  CAS  ADS  Google Scholar 

  17. Pigot, A. L., Owens, I. P. F. & Orme, C. D. L. Speciation and extinction drive the appearance of directional range size evolution in phylogenies and the fossil record. PLoS Biol. 10, e1001260 (2012)

    Article  CAS  Google Scholar 

  18. Sepkoski, D. Rereading the Fossil Record (Univ. Chicago Press, 2012)

  19. Nee, S. Birth–death models in macroevolution. Annu. Rev. Ecol. Evol. Syst. 37, 1–17 (2006)

    Article  Google Scholar 

  20. Shanahan, T. Phylogenetic inertia and Darwin’s higher law. Stud. Hist. Philos. Biol. Biomed. Sci. 42, 60–68 (2011)

    Article  Google Scholar 

  21. Bovet, P. & Benhamou, S. Spatial analysis of animals’ movements using a correlated random walk model. J. Theor. Biol. 131, 419–433 (1988)

    Article  Google Scholar 

  22. Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859)

  23. Eldredge, N. & Gould, S. J. in Models in Paleobiology (ed. Schopf, T. J. M. ) 82–115 (Freeman, Cooper and Co., 1972)

  24. Raup, D. M. & Sepkoski, J. J. Jr. Mass extinctions in the marine fossil record. Science 215, 1501–1503 (1982)

    Article  CAS  ADS  Google Scholar 

  25. Stenseth, N. C. & Maynard Smith, J. Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38, 870–880 (1984)

    Article  Google Scholar 

  26. Ezard, T. H., Aze, T., Pearson, P. N. & Purvis, A. Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science 332, 349–351 (2011)

    Article  CAS  ADS  Google Scholar 

  27. Vermeij, G. J. & Roopnarine, P. D. Reining in the Red Queen: the dynamics of adaptation and extinction reexamined. Paleobiology 39, 560–575 (2013)

    Article  Google Scholar 

  28. Voje, K. L., Holen, O. H., Liow, L. H. & Stenseth, N. C. The role of biotic forces in driving macroevolution: beyond the Red Queen. Proc. R. Soc. Lond. B 282, 20150186 (2015)

    Article  Google Scholar 

  29. Liu, L . et al. Dental functional traits of mammals resolve productivity in terrestrial ecosystems past and present. Proc. R. Soc. Lond. B 279, 2793–2799 (2012)

    Article  Google Scholar 

  30. Žliobaite˙, I. et al. Herbivore teeth predict climatic limits in Kenyan ecosystems. Proc. Natl Acad. Sci. USA 113, 12751–12756 (2016)

    Article  Google Scholar 

  31. Jernvall, J. & Fortelius, M. Common mammals drive the evolutionary increase of hypsodonty in the Neogene. Nature 417, 538–540 (2002)

    Article  CAS  ADS  Google Scholar 

  32. Hannisdal, B., Haaga, K. A., Reitan, T., Diego, D. & Liow, L. H. Common species link global ecosystems to climate change. Proc. R. Soc. Lond. B 284, 20170722

  33. Hull, P. M., Darroch, S. A. F. & Erwin, D. H. Rarity in mass extinctions and the future of ecosystems. Nature 528, 345–351 (2015)

    Article  CAS  ADS  Google Scholar 

  34. Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, 1995)

  35. Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. Predicting extinction risk in declining species. Proc. R. Soc. Lond. B 267, 1947–1952 (2000)

    Article  CAS  Google Scholar 

  36. Steininger, F. F . et al. in The Evolution of Western Eurasian Neogene Mammal Faunas (eds Bernor, R. L. et al.) 7–46 (Plenum, 1996)

  37. Fortelius, M. et al. An ecometric analysis of the fossil mammal record of the Turkana Basin. Phil. Trans. R. Soc. Lond. B 371, 20150232 (2016)

    Article  Google Scholar 

  38. Eronen, J. T., Evans, A. R., Fortelius, M. & Jernvall, J. Genera are often better than species for detecting evolutionary change in the fossil record: a reply to Salesa et al. Evolution 65, 1514–1516 (2011)

    Article  Google Scholar 

  39. Gaston, K. J. et al. Abundance–occupancy relationships. J. Appl. Ecol. 37 (Suppl.), 39–59 (2000)

    Article  Google Scholar 

  40. Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1944)

  41. Fortelius, M. et al. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evol. Ecol. Res. 4, 1005–1016 (2002)

    Google Scholar 

  42. Eronen, J. T. et al. Precipitation and large herbivorous mammals I: estimates from present-day communities. Evol. Ecol. Res. 12, 217–233 (2010)

    Google Scholar 

Download references


I.Ž. and M.F. acknowledge funding from the Finnish Academy (ECHOES project). M.F. was the recipient of a research award from the Alexander von Humboldt Foundation. N.C.S. has been funded by the Research Council of Norway via CEES. We thank H. Mannila for seminal explorations of the law as well as members of the Björn Kurtén Club (University of Helsinki) and participants of the workshops on ‘Biotic Drivers of Macroevolution’ organized by CEES (Colloquium 4) for discussions on macroevolution. This Letter is a contribution from the Valio Armas Korvenkontio Unit of Dental Anatomy in Relation to Evolutionary Theory. We miss L. Van Valen and are grateful for the discussions we had with him over many years.

Author information

Authors and Affiliations



I.Ž. and M.F. developed the theory. I.Ž. did the modelling and computational experiments. All authors analysed the results. I.Ž. and M.F. wrote the initial text and all authors contributed to the final text. N.C.S. initiated collaborative analysis to detect biotic and abiotic drivers in the fossil record, which inspired this paper.

Corresponding author

Correspondence to Indrė Žliobaitė.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Extended data figures and tables

Extended Data Table 1 Characteristics of the North American dataset
Extended Data Table 2 Characteristics of the European dataset
Extended Data Table 3 Characteristics of the Turkana dataset
Extended Data Table 4 The North American dataset
Extended Data Table 5 The European dataset
Extended Data Table 6 The Turkana dataset

Supplementary information

Life Sciences Reporting Summary (PDF 83 kb)

Supplementary Information

This file contains figures S1-S5 and tables S1-S11. (PDF 2524 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Žliobaitė, I., Fortelius, M. & Stenseth, N. Reconciling taxon senescence with the Red Queen’s hypothesis. Nature 552, 92–95 (2017).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing