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

Abstract

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.

The role of biotic forces in driving macroevolution: beyond the Red Queen

“…[26,29,30,32]). Indeed, the original Red Queen metaphor suggests that all species have to continuously evolve so as not to lag behind other species and that they have constant (age-independent) probabilities of extinction.…”

“…Abiotic disturbances are commonly argued to be the major causes of extinction by palaeontologists [1,3,4,6,11,32]. This view is shared by Vermeij's escalation hypothesis, which claims that strong competitors rarely drive their enemies to complete extinction, as poor competitors usually are able to sustain viable populations in physiologically marginal environments.…”

Quasi-static Eocene–Oligocene climate in Patagonia promotes slow faunal evolution and mid-Cenozoic global cooling

“…climate and M A N U S C R I P T ACCEPTED MANUSCRIPT 5 tectonics; so-called -Court Jester‖-type hypotheses; Barnosky, 2001). The Red Queen has recently been demoted as being of limited use to explain adaptation or extinction, based on both theoretical and empirical considerations (Vermeij and Roopnarine, 2013), and many deep-time studies in both North and South America point to climate as a major driver of evolution, in support of Court Jester hypotheses (Barnosky, 2001;Barnosky et al, 2003;Figueirido et al, 2012;Woodburne et al, 2014). In contrast, other comparative work fails to show any relation between environmental alteration and faunal change (Prothero, 1999(Prothero, , 2004Alroy et al, 2000); thus the importance of the Court Jester for major evolutionary trends in faunas remains uncertain.…”

Interdependence of specialization and biodiversity in Phanerozoic marine invertebrates

“…This debate has been dichotomized into two hypotheses, namely the Red Queen (biotic factors) and the Court Jester (abiotic factors). Irrespective of recent criticism of the Red Queen metaphor as a general description of evolutionary dynamics 41 , a consensus is forming that biotic and abiotic aspects are not mutually exclusive 3,11,42 . For example, the speciation of Cenozoic planktonic foraminifera was more strongly shaped by biotic variables than abiotic change, whereas the opposite was true for extinction 42 .…”