From descent with modification to the origins of novelty

Highlights

• Descent with modification is the foundation of all of evolutionary biology.

• Yet evolutionary novelties are defined as lacking affinities to structures that already existed in the ancestral state, i.e. to somehow emerge in the absence of homology.

• The development of insect wings, beetle horns, and other diverse traits relies on the same ancestral, homologous gene regulatory network and associated tissues.

• Discoveries such as these call for a reassessment of the usefulness of defining evolutionary novelty as necessitating the absence of homology.

• Instead we need to direct attention to how ancestral homologies bias innovation to facilitate hotspots in some places, and deep conservation elsewhere.

Abstract

Descent with modification is the foundational framework of all of evolution. Yet evolutionary novelties are defined as lacking affinities to structures that already existed in the ancestral state, i.e. to somehow emerge in the absence of homology. We posit that reconciling both perspectives necessitates the existence of a type of innovation gradient that allows descent with modification to seed the initiation of a novel trait, which once in existence can then diversify into its variant forms. Recent work on diverse, textbook examples of morphological novelties illustrate the value of the innovation gradient concept. Innovations as profound and diverse as insect wings, beetle horns, and treehopper helmets derive from homologous source tissues instructed in their development by homologous gene regulatory networks. Yet rather than rendering these traits no longer novel, we posit that discoveries such as these call for a reassessment of the usefulness of defining evolutionary novelty as necessitating the absence of homology. Instead, we need to redirect our attention to how ancestral homologies scaffold and bias the innovation gradient to facilitate hotspots of innovation in some places, and deep conservation elsewhere.