Reconciling taxon senescence with the Red Queen’s hypothesis

Abstract

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.

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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.

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Acknowledgements

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.

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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.

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Correspondence to Indrė Žliobaitė.

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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

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Žliobaitė, I., Fortelius, M. & Stenseth, N. Reconciling taxon senescence with the Red Queen’s hypothesis. Nature 552, 92–95 (2017). https://doi.org/10.1038/nature24656

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