Bring back the phenotype

Abstract

When thinking about evolutionary change, many practicing biologists will focus on changes in allele frequencies over time. This gene-centric view of evolution has strongly impacted how evolution (and biological science in general) is thought of, taught, and funded. In this viewpoint, we join recent criticisms of the gene-centric view and call for reinstalling a phenotypic view of evolution. The assumptions of the gene-centric view-enormous/nonstructured populations and totally random interactions between genes, individuals, and environments-are hard to imagine in the real world. A gene's effects on phenotype and fitness depend on its interactions with other genes (epistasis), other individuals, the microbiome, and the environment, and it changes between generations, populations, and environments. Incorrectly, genes have been given an agency and role in natural selection that they do not possess: they replicate, but they do not have phenotypic variation or differential proliferation through their traits (these are characteristics of the units of selection deemed 'interactors'). Here, we show how a phenotypic view of evolution is necessary to capture several widespread phenomena: epistasis, nongenetic inheritance, multilevel selection, and niche construction through plant-soil feedbacks, all of which have vast empirical evidence. Life is marvelous, complex, and certainly more than machinery and genetic information.

Keywords: adaptationist bias; epistasis; gene‐centric view; multilevel selection; niche construction; nongenetic inheritance; phenotype; units of selection.