Cracking open the blackbox of genotype–phenotype map: crossing the explanatory gap between micro- and macroevolution

A key insight of evolutionary genetics is that the evolvability of a population depends crucially on the amount and distribution of heritable phenotypic variation across traits. Because this insight focuses on segregating variation, the traits that do not vary among individuals but differ among higher taxa are ignored. Slowly evolving traits, like body plan organization and homologs, are nevertheless essential because they set the phenotypic boundary conditions within which variation segregates. Therefore, understanding long-term evolutionary change requires understanding the principles that control variation in varying AND conserved traits, in addition to understanding how drift and selection influence segregating population variation. In this perspective, I propose that this understanding is attainable if we acknowledge that different processes, which map sequence variation to phenotypic variation, have different capacities to produce variation and evolve. I suggest decomposing the GP map according to types of processes with different variational properties. For vertebrates, these are morphogenesis, growth, and maintenance. This perspective allows us to focus on how these processes interact under the influence of natural selection and delineate the conditions leading to different patterns of evolutionary change.