Fitness as the organismal performance measure guiding adaptive evolution

Abstract

A long-standing problem in evolutionary theory is to clarify in what sense (if any) natural selection cumulatively improves the design of organisms. Various concepts, such as fitness and inclusive fitness, have been proposed to resolve this problem. In addition, there have been attempts to replace the original problem with more tractable questions such as whether a given gene or trait is favoured by selection. Here we ask what theoretical properties the concept fitness should possess to encapsulate the improvement criterion required to talk meaningfully about adaptive evolution. We argue that natural selection tends to shape phenotypes based on the causal properties of individuals, and that this tendency is therefore best captured by a fitness concept that focusses on these properties. We highlight a fitness concept which meets this role under broad conditions, but requires adjustments in our conceptual understanding of adaptive evolution. These adjustments combine elements of Dawkinsian gene selectionism and Egbert Leigh’s “parliament of genes”.