Phenotypic Novelty in EvoDevo: The Distinction Between Continuous and Discontinuous Variation and Its Importance in Evolutionary Theory

Abstract

The introduction of novel phenotypic structures is one of the most significant aspects of organismal evolution. Yet the concept of evolutionary novelty is used with drastically different connotations in various fields of research, and debate exists about whether novelties represent features that are distinct from standard forms of phenotypic variation. This article contrasts four separate uses for novelty in genetics, population genetics, morphology, and behavioral science, before establishing how novelties are used in evolutionary developmental biology (EvoDevo). In particular, it is detailed how an EvoDevo-specific research approach to novelty produces insight distinct from other fields, gives the concept explanatory power with predictive capacities, and brings new consequences to evolutionary theory. This includes the outlining of research strategies that draw attention to productive areas of inquiry, such as threshold dynamics in development. It is argued that an EvoDevo-based approach to novelty is inherently mechanistic, treats the phenotype as an agent with generative potential, and prompts a distinction between continuous and discontinuous variation in evolutionary theory.

Why an extended evolutionary synthesis is necessary

“…the phenotypic outcome is only indirectly related to genetic variation and yet still follows predictable pathways. In other words, the variational range of a population is not defined merely by genetic variation but by the developmental system as a whole, providing sources of phenotypic bias and novelty [ 24 , 74 ]. It is now possible to determine the relative importance of natural selection and of genetic and developmental determinants of organic diversity [ 55 ].…”

“…Phenotypic accommodation may be followed by genetic accommodation and thus result in more rapid adaptation to novel environments [ 79 ]. The effect of a novel environment on phenotypic plasticity may be coupled with simultaneous exposure of ‘hidden’ developmental variation and strong selection on this variation [ 82 ] and could provide a starting point for the evolutionary persistence of phenotypic innovations [ 24 ]. Plasticity has also been linked to the ubiquitous phenomenon of homoplasy [ 83 ] and to rapid divergence of phylogenetic lineages [ 21 ].…”

Interspecific allometry for sexual shape dimorphism: Macroevolution of multivariate sexual phenotypes with application to Rensch's rule

“…Finally, because is derived from a phenotypic distance, one could, in theory, use the approach to characterize patterns of sexual dimorphism in non‐continuous traits, and determine quantitatively whether the degree of sexual dimorphism is enhanced with increasing body size. Across the tree of life, major phenotypic adaptations are often described as evolutionary innovations or novelties (sensu Wagner and Altenberg 1996; Wagner and Muller 2002; Peterson and Müller 2016), where these changes are characterized as discrete shifts from one phenotypic state to another (e.g., Holliday and Gardner 2012; O'Keefe et al. 2011).…”

Prospects for a General Theory of Evolutionary Novelty

“…Other recent studies of evolutionary novelty have focused on the generation of morphological variation rather than ecological opportunity. Where Darwin, Mayr, and others linked form and function, many of those in the evo-devo community sheared the two issues, focusing on form, and particularly on the origin of new, homologous characters as the basis of novelty (Muller and Wagner, 1991;Moczek, 2008;Pigliucci, 2008;Peterson and Muller, 2016).…”