Origin of the fittest: Link between emergentvariation and evolutionary change as acritical question in evolutionary biology

Abstract

In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions inprotein networks and emergent developmental processes can delineate the directions of evolutionarychange, including the opportunity for natural selection. These effects are reflected in the evolution of developmentalprogrammes that link genomic architecture with a corresponding functioning phenotype. Tworecent findings call for closer examination of the rules by which these links are constructed. First is the realizationthat high dimensionality of genotypes and emergent properties of autonomous developmentalprocesses (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypicand genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conservedgene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generativeprocesses. Establishing the causal reciprocal links between ongoing neutral expansion of genomicarchitecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversificationtherefore becomes an important goal of evolutionary biology and is the latest reincarnation of thesearch for a framework that links development, functioning and evolution of phenotypes. Here I examine,in the light of recent empirical advances, two evolutionary concepts that are central to this framework-naturalselection and inheritance-the general rules by which they become associated with emergentdevelopmental and homeostatic processes and the role that they play in descent with modification. © 2011 The Royal Society.