How Do Morphological Novelties Evolve? Novel Approaches to Define Novel Morphologies

Abstract

Evolutionary innovations are biological revolutions: new organs are critically associated with the emergence of new species and their exploitation of new niches. Despite their importance in the history of life, how a morphological novelty arises and evolves is a long-standing question in evolutionary biology. By combining evolutionary theories with comparative developmental embryology, the emergence of the evo-devo discipline at the end of the twentieth century revived the interest in these questions. Mostly, a lack of appropriate techniques for non-model organisms precluded further advancements, and it is only now that novel DNA sequencing and genome editing techniques allow us to ask these long-standing questions in the organisms that may best serve to answer them. These new approaches have revealed the need of a new conceptual framework to define and classify morphological novelties in animal evolution. Thus, in this review, we will first revisit some of the most influential definitions of morphological novelty that have been coined over the last half century to further propose the use of the generative events that originated a new structure as the criterion to consider this new organ a morphological novelty or not. These generative events or phenomenological modes are divided into four different categories: (1) fusion of existing structures, (2) heterotopic activation of a gene regulatory network, (3) recruitment of additional cell types (either pre-existing or novel) into structures and (4) processes of symbiogenesis. We will finally revisit how recent studies have shed light into the mechanisms underpinning the evolutionary origin of some of the most classical morphological novelties.