Reconciling taxon senescence with the Red Queen’s hypothesis

Focusing attention on the expansion of taxa, rather than their survival, resolves the apparent contradiction between seemingly deterministic patterns of waxing and waning of taxa over time and the randomness of extinction implied by the Red Queen’s hypothesis. Predicting extinction at the tip of a hat According to Leigh Van Valen's 'Red Queen' hypothesis, predators are always looking for an edge on their prey, which in turn evolve to evade them. Van Valen was investigating extinction, back when people thought that species became extinct when they ran out of puff, and suggested that it was more probabilistic, with no correlation between the age of a taxon and its risk of extinction. However, extensive sampling shows that the abundance of taxa through time has a hat-like distribution (scarce at the beginning and end with a peak in the middle), which, if correct, would imply that the correlation exists. Indrė Žliobaitė and colleagues modelled speciation and extinction using a random walk constrained by resources and uncovered a unimodal 'hat' pattern. They suggest that a species at its peak is limited by competition, whereas its initial diversification and eventual extinction are limited by random environmental effects. Therefore, efforts to predict a species' risk of extinction should look at when it is just past its peak. 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 extinction 1 , 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 mammals 2 , 3 , 4 , marine invertebrates 5 , 6 , 7 , marine microorganisms 8 , and recent Hawaiian clades of animals and plants 9 . 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 hypothesis 1 , 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 th