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.

Keywords: EvoDevo; Evolutionary theory; Innovation; Macroevolution; Phenotypic novelty.

Fig. 1

Finite element modeling of the upper pharyngeal jaw novelty in the cichlid Amatitlania nigrofasciata. A volume rendering of the fish, 6 days post fertilization, and associated musculature has been added to give spatial reference to the upper pharyngeal jaw. Small window The fish is shown slightly forward of the pectoral girdle, with one half cut away. Magnified area is outlined in white. Large window Muscles affecting pharyngeal jaw adduction are shown in red. The upper pharyngeal jaw is shown in blues and greens indicating various levels of von Mises stress. These types of models can determine the location, orientation, and magnitude of biomechanical signals during development. a retractor dorsalis; b transversus dorsalis posterior; c levator posterior; d upper pharyngeal jaw; e obliquus dorsalis; f levator internus lateralis; g levator externus 4; h transversus dorsalis anterior; i levator internus medialis

Fig. 2

Population level spread of a discontinuous trait (a) versus spread from a single (mutant) individual (b). Circles represent individuals without the novelty; triangles represent individuals with the novelty. The figure demonstrates hypothetical general patterns of novelty origination and is not meant to represent accurate ratios of novelty versus ancestral traits, likelihood of events, etc. a A developmental parameter can undergo continuous variation, represented here as variable grey scale value, which leads to the same adult structure, represented here as a circle. If the variation crosses a threshold level, a discontinuous change resulting in a qualitatively new phenotype occurs, represented here as a triangle. As the novelty is determined by the developmental system and is in another dimension than the threshold that creates it, their symbols are purposely incommensurable (shapes and colors). In each successive generation, natural selection pushes the population towards the threshold (such as a biomechanical signal, morphogen patterning process, etc.) shown by the circles becoming darker. By F3, some individuals have crossed the threshold. By F4, more individuals have crossed the threshold. Since the threshold is determined by properties of the phenotype and does not necessarily depend on one particular gene, many different gene combinations may be involved in passing the threshold. Loss of individual genetic lines through death, no mating, etc., do not hinder the spread of the novelty as other individuals are close to the same threshold. Similarly, variation away from the threshold (represented by asterisk) does not put the entire population at risk for loss of the novelty. Importantly, the critical threshold is approached only by coincidence, and the selection pressure on the trait is unrelated to the existence of a threshold. b Origination of novelty from a specific gene mutation is spread only from the individual with the mutation, and relies on positive selection for that novelty as opposed to selection on another trait that has a threshold. Several factors can cause loss of the trait. “Allele”: Offspring may inherit the allele without the novel mutation. “Loss”: Individuals with the novel mutation may die during development or before they have a chance to mate. “No symbol”: Inability to produce viable offspring or find a mate. “Reversal”: Individuals may inherit the novel mutation, but in a different genetic background it may not result in the novel phenotype. The latter possibility may allow the gene to be retained in the gene pool, but there is no selection pressure for its maintenance. The other possibilities remove the gene. In the initial generations after the gene mutation, the small number of individuals with the mutation and the large number of ways in which it can be lost make it less likely to be spread than in the population level dynamic shown in a. Critically, case b requires positive selection (or drift) on a novel gene that is able to spread throughout a population, while case a has the entire population primed for the introduction of a novelty, which can occur with the genes already present in the gene pool

Fig. 3

Schematic connecting the processes of innovation and adaptation. i Adaptation. A preexisting element is the starting source for adaptive change. Natural selection acting on heritable variation determines the form of the phenotype. This works through continuous variation, with small changes in each generation resulting in an adaptive trait present in the population. ii Innovation. The initial source for innovation is the configuration of the developmental system, including both epigenetic and genetic factors. Epigenetic in this case refers to traits and processes above the gene level, such as environmental factors, tissue interactions, biomechanical forces, etc. A developmental property, such as cartilage induction by compression, determines the form that occurs from the developmental configuration. In the case of novelties, this form appears as discontinuous variation of the phenotype compared to previous generations. The resulting novelty, a new homologue, can undergo further adaptation. Part i represents the striped borders and part ii the solid black borders in Fig. 4

Fig. 4

Schematic for the evolutionary introduction of three kinds of phenotypic novelties concurrent with variational change. Each section of A-H represents a single individual in a population that is experiencing morphological evolution, with each sequential section representing the next morphology. The type of evolution of a single structure is denoted by striped, white, or black outlines. Striped outlines indicate qualitatively discontinuous phenotypic change arising in a direction determined by the developmental system. This corresponds to Fig. 3 ii (Innovation). Solid black outlines indicate quantitative phenotypic change determined by natural selection. This corresponds to Fig. 3 i (Adaptation). White borders show phenotypic stasis. a Establishment of a new multicellular body assembly, a T1 novelty. b Body plan undergoes quantitative change. c Body plan continues to undergo quantitative change, while a qualitatively new structural unit, a T2 novelty, is added. d Body plan is stasis while the new structure undergoes quantitative change. e Body plan evolves quantitatively, structural unit is in stasis, and a new T2 unit is added to the body plan. f Body plan is in stasis, both structural units are undergoing quantitative change. g Body plan evolves quantitatively, a new structural unit is added, the first structural unit is in stasis, and the second structural unit has quantitative change in a qualitatively new dimension, a T3 novelty. h Body plan is in stasis. The first structural unit undergoes quantitative change, and passes a threshold to create a T2 novelty. The second structural unit is in stasis. The third structural unit experiences quantitative change