Adaptive dynamics under development-based genotype–phenotype maps

Abstract

It is not known whether natural selection can encounter any given phenotype that can be produced by genetic variation. There has been a long-lasting debate about the processes that limit adaptation and, consequently, about how well adapted phenotypes are. Here we examine how development may affect adaptation, by decomposing the genotype-fitness map-the association between each genotype and its fitness-into two: one mapping genotype to phenotype by means of a computational model of organ development, and one mapping phenotype to fitness. In the map of phenotype and fitness, the fitness of each individual is based on the similarity between realized morphology and optimal morphology. We use three different simulations to map phenotype to fitness, and these differ in the way in which similarity is calculated: similarity is calculated for each trait (in terms of each cell position individually), for a large or a small number of phenotypic landmarks (the 'many-traits' and 'few-traits' phenotype-fitness maps), and by measuring the overall surface roughness of morphology (the 'roughness' phenotype-fitness map). Evolution is simulated by applying the genotype-phenotype map and one phenotype-fitness map to each individual in the population, as well as random mutation and drift. We show that the complexity of the genotype-phenotype map prevents substantial adaptation in some of the phenotype-fitness maps: sustained adaptation is only possible using 'roughness' or 'few-traits' phenotype-fitness maps. The results contribute developmental understanding to the long-standing question of which aspects of phenotype can be effectively optimized by natural selection.

Evolving phenotypic networks in silico

“…The issue is that we do not have (yet) a proper formalism to answer such questions: among other problems and despite recent advances (see e.g. [9][10][11]) the nature of the mapping between phenotype and genotype is still an open question. For this reason, we turn to computational approaches and propose a generic in silico evolution procedure to "predict" what kind of networks can evolve to perform a given biological function [12,13].…”

Quantitative genetics provides predictive power for paleontological studies of morphological evolution

“…In recent years, startling advances have been made in our understanding of the molecular mechanisms of development and the genomic structures that underpin them. Laboratory manipulations are able to determine the patterns of gene expression that produce phenotypic structures such as brains, bones, and teeth (2,3); computational models of the spatial dynamics of development are capable of predicting the phenotypic outcomes of up-or down-regulation of gene expression (4); and genomic analyses reveal the regulatory mechanisms that govern cascades of gene expression (5). These tools have mapped the causal links between genotype and phenotype that were largely missing from 20th century evolutionary biology.…”

Shared developmental programme strongly constrains beak shape diversity in songbirds

“…Therefore, our findings are consistent with a hypothesis that beak shapes in the birds we studied thus far are, in fact, biased by the beak morphogenetic process, which is dependent on the controlled growth zone decay despite reported high flexibility in the usage of particular molecular pathways and exact tissue modules in different species of songbirds, including those in our study 11,12,14,20,30,31 . We argue that beak phenotypic variation in songbirds could be evolving under a strong developmental constraint under its accepted current definitions 6,[32][33][34][35] .…”

“…Interestingly, an alternative point of view 5 suggests that beak shape diversity mainly results from morphogenetic processes independent of adaptation, with constraints being largely imposed by the beak developmental programme. Within this hypothesis, beak phenotypic variation and morphological adaptation would be limited or strongly biased by the structure and dynamics of its developmental programme 6 . Both extrinsic and intrinsic factors are expected to play a role in shaping morphological diversity.…”