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Reining in the Red Queen: the dynamics of adaptation and extinction reexamined

Published online by Cambridge University Press:  09 July 2013

Geerat J. Vermeij  and
Peter D. Roopnarine
Geerat J. Vermeij
Affiliation:
Department of Geology, One Shields Avenue, University of California Davis, Davis, California 95616, U.S.A. E-mail: gjvermeij@ucdavis.edu
Peter D. Roopnarine
Affiliation:
Department of Invertebrate Zoology and Geology, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, California 94118, U.S.A. E-mail: proopnarine@calacademy.org. Corresponding author
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Abstract

One of the most enduring evolutionary metaphors is Van Valen's (1973) Red Queen. According to this metaphor, as one species in a community adapts by becoming better able to acquire and defend resources, species with which it interacts are adversely affected. If those other species do not continuously adapt to compensate for this biotically caused deterioration, they will be driven to extinction. Continuous adaptation of all species in a community prevents any single species from gaining a long-term advantage; this amounts to the Red Queen running in place. We have critically examined the assumptions on which the Red Queen metaphor was founded. We argue that the Red Queen embodies three demonstrably false assumptions: (1) evolutionary adaptation is continuous; (2) organisms are important agents of extinction; and (3) evolution is a zero-sum process in which living things divide up an unchanging quantity of resources. Changes in the selective regime need not always elicit adaptation, because most organisms function adequately under many “suboptimal” conditions and often compensate by demonstrating adaptive flexibility. Likewise, ecosystems are organized in such a way that they tend to be robust and capable of absorbing invasions and extinctions, at least up to a point. With a simple evolutionary game involving three species, we show that Red Queen dynamics (continuous adaptation by all interacting species) apply in only a very small minority of possible outcomes. Importantly, cooperation and facilitation among species enable competitors to increase ecosystem productivity and therefore to enlarge the pool and turnover of resources. The Red Queen reigns only under a few unusual circumstances.

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Paleobiology , Volume 39 , Issue 4 , Fall 2013 , pp. 560 - 575
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Copyright © The Paleontological Society 

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