Aligning functional network constraint to evolutionary outcomes

Abstract

It is likely that there are constraints on how evolution can progress, and well-known evolutionary phenomena such as convergent evolution, rapid adaptation, and genic evolution would be difficult to explain under the absence of any such evolutionary constraint. One dimension of constraint results from a finite number of environmental conditions, and thus natural selection scenarios, leading to convergent phenotypes. This limits which genetic variants are adaptive, and consequently, constrains how variation is inherited across generations. Another, less explored dimension of evolution is functional constraint at the molecular level. Some widely accepted examples for this dimension of evolutionary constraint include genetic linkage, codon position, and architecture of developmental genetic pathways, that together constrain how evolution can shape genomes through limiting which mutations can increase fitness. Genomic architecture, which describes how all gene products interact, has been discussed to be another dimension of functional genetic constraint. This notion had been largely discredited by the modern synthesis, especially because macroevolution was not always found to be perfectly deterministic. But debates on whether evolutionary constraint stems mostly from environmental (extrinsic) or genetic (intrinsic) factors have mostly been held at the intellectual level using sporadic evidence. Quantifying the relative contributions of these different dimensions of constraint is, however, fundamentally important to understand the mechanistic basis of seemingly deterministic evolutionary outcomes. In some model organisms, genetic constraint has already been quantitatively explored. Forays into testing the relationship between genomic architecture and evolution included studies on protein evolutionary rate variation in essential versus nonessential genes, and observations that the number of protein interactions within a cell (gene pleiotropy) determines the fitness effect of mutations. In this contribution, existing evidence for functional genetic constraint as shaping evolutionary outcomes is reviewed and testable hypotheses are defined for functional genetic constraint influencing (i) convergent evolution, (ii) rapid adaptation, and genic adaptation. An analysis of the yeast interactome incorporating recently published data on its evolution, reveals new support for the existence of genomic architecture as a functional genetic dimension of evolutionary constraint. As functional genetic networks are becoming increasingly available, evolutionary biologists should strive to evaluate functional genetic network constraint, against variables describing complex phenotypes and environments, for better understanding commonly observed deterministic patterns of evolution in non-model organisms. This may help to quantify the extrinsic versus intrinsic dimensions of evolutionary constraint, and result in a better understanding of how fast, effectively, or deterministically organisms adapt.\n\nGlossary