Why call it developmental bias when it is just development?

Abstract

The concept of developmental constraints has been central to understand the role of development in morphological evolution. Developmental constraints are classically defined as biases imposed by development on the distribution of morphological variation.This opinion article argues that the concepts of developmental constraints and developmental biases do not accurately represent the role of development in evolution. The concept of developmental constraints was coined to oppose the view that natural selection is all-capable and to highlight the importance of development for understanding evolution. In the modern synthesis, natural selection was seen as the main factor determining the direction of morphological evolution. For that to be the case, morphological variation needs to be isotropic (i.e. equally possible in all directions). The proponents of the developmental constraint concept argued that development makes that some morphological variation is more likely than other (i.e. variation is not isotropic), and that, thus, development constraints evolution by precluding natural selection from being all-capable.This article adds to the idea that development is not compatible with the isotropic expectation by arguing that, in fact, it could not be otherwise: there is no actual reason to expect that development could lead to isotropic morphological variation. It is then argued that, since the isotropic expectation is untenable, the role of development in evolution should not be understood as a departure from such an expectation. The role of development in evolution should be described in an exclusively positive way, as the process determining which directions of morphological variation are possible, instead of negatively, as a process precluding the existence of morphological variation we have no actual reason to expect.This article discusses that this change of perspective is not a mere question of semantics: it leads to a different interpretation of the studies on developmental constraints and to a different research program in evolution and development. This program does not ask whether development constrains evolution. Instead it asks questions such as, for example, how different types of development lead to different types of morphological variation and, together with natural selection, determine the directions in which different lineages evolve.

Keywords: Development; Developmental bias; Developmental constraints; Developmental mechanisms; Morphogenesis; Morphological evolution; Variational properties.

Fig. 1

The direction of morphological evolution. a Example of a two-trait morphospace considering, for example, limb length (X-axis) and width (Y-axis). Each point in such morphospace represents an individual limb morphology in a population. The gray point represents the population mean for both traits. b Example of evolution in a morphological direction in the limb morphospace The gray areas represent the distribution of the individuals of a population at different successive generations. The arrows show the direction of evolution between generations (a vector from each generation mean to the next generation mean). c Arrows show a sample of the directions of possible morphological variation under the isotropic expectation for a two-trait morphospace. d Example of a fitness landscape on the same two-trait limb morphospace. The contour lines show points, i.e. limb morphologies, with the same fitnes (the higher the fitness the thicker the line). In this example morphological variation is isotropic so the population can go from any point in the morphospace to any other nearby point. As a result one can deduce how morphology will change based on the fitness landscape: the population would evolve towards the steepest peak. The gray line shows that this is the evolutionary trajectory the population would follow. d As in C but in this case morphological variation is not isotropic. The gray regions show the morphologies, i.e. points in the morphospace, that are possible by changes in development (the darker the point the more likely it is to arise from changes in development). In this case, as shown by the trajectory in white, the population would not evolve towards the steepest fitness peak because there is no morphological variation in that direction

Fig. 2

Developmental mechanisms, initial and final morphology. a Example of an initial morphology. Cylinders represent epithelial cells. Cells in yellow express a gene that is not expressed in the cells in blue. All blue cells express the same genes. b Example of a developmental mechanism. Balls represent gene products. Red balls are extracellular diffusive gene products (a signal). Gene 2 is the gene expressed by the cells in yellow in a. For simplicity the signal transduction pathway is not represented. Green arrows represent positive regulation. Red cells represent negative regulation. Squares represent cell behaviors or cell mechanical properties. c Three examples of final morphologies arising from the initial morphology in a through the developmental mechanism in b (according to a mathematical general model of development called EmbryoMaker [45]). The morphological variation is the one arising from variation in the amount of signal being secreted (the signal is gene 1). The variation is mostly in the overall curvature of the epithelium. There is a default cell division rate in all cells. As in a cylinders represent epithelial cells, color represents z-axis coordinate values as in a topographic map. d. As in c but for the three final morphologies arising from variation in the diffusivity of the signal. The morphologies vary in how the curvature decreases with the distance to the signal’s source. In the morphology in the upper row the curvature is very strong near the cells secreting the signal. In the morphology in the lower row, the curvature is more evenly distributed (low row) (e) as in a. f As in b but for a different developmental mechanism. The gene that yellow cells in d express is gene 2. g Three examples of final morphologies arising from the initial morphology in d through the developmental mechanism in e (also according to EmbryoMaker)