Prometheus and Proteus: the creative, unpredictable individual in evolution

Evolution and Cognition 1:101-129 (1992)
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Abstract

Evolutionary theory usually neglects two variables: the changes induced in the environment by the evolving organism, and individual uniqueness in sexually reproducing species. In order to fuel its maintenance and reproduction, an organism must average a positive net energy balance vis-a-v}s its environment. It achieves this via aptations, which consist of information (i.e., the internalization of all that is predictable about the environment, including the machinery to take advantage of this information) and stored energy (to operate the machinery, including a safety margin to deal with events that are unpredictable in principle). Taking advantage of a prediction, however, interferes with what has been predicted; each adaptation by the organism therefore changes its environmental target. Today's organism is adapted to yesterday's environment, and today's predator inherits yesterday's prey image. This paper attempts to show that, over evolutionary time, the persistence of this asymmetric, time-lagged relationship is owed increasingly to genetically unique individuals. Individual uniqueness as resulting from sexual reproduction is janusfaced. It endows an evolving population with both a forward-looking (promethean) and backward-looking (protean) feature. A population made up of genetically unique individuals is promethean (creative) in its ability to exploit non-homogeneous resources and respond serendipitously to environmental change via new genotypes; it is protean (elusive) in presenting a pursuer (predator or parasite) with a scattered target. Furthermore, because of the asymmetry between the winnowing of the target gene pool by the pursuer, and the genetic fixation in the pursuer of an outdated target image, the target keeps evolving away from the pursuer at a speed and in a direction that are a function of the pursuer's success. This mechanism ensures an evolutionary time lag be102 W. Sterrer tween pursuer and target, which explains escalation, the stability of asymmetric coevolutionary systems such as the life/dinner principle, and the pervasiveness of the Red Queen effect. Individuality thus both promotes and retards the speed of evolution. Having probably originated simultaneously with predation, sex-generated individuality is a self-accelerating evolutionary process that may account for much of today's organismic and environmental complexity.

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