Bias in the arrival of variation can dominate over natural selection in Richard Dawkins’s biomorphs

Biomorphs, Richard Dawkins’s iconic model of morphological evolution, are traditionally used to demonstrate the power of natural selection to generate biological order from random mutations. Here we show that biomorphs can also be used to illustrate how developmental bias shapes adaptive evolutionary outcomes. In particular, we find that biomorphs exhibit phenotype bias, a type of developmental bias where certain phenotypes can be many orders of magnitude more likely than others to appear through random mutations. Moreover, this bias exhibits a strong preference for simpler phenotypes with low descriptional complexity. Such bias towards simplicity is formalised by an information-theoretic principle that can be intuitively understood from a picture of evolution randomly searching in the space of algorithms. By using population genetics simulations, we demonstrate how moderately adaptive phenotypic variation that appears more frequently upon random mutations can fix at the expense of more highly adaptive biomorph phenotypes that are less frequent. This result, as well as many other patterns found in the structure of variation for the biomorphs, such as high mutational robustness and a positive correlation between phenotype evolvability and robustness, closely resemble findings in molecular genotype-phenotype maps. Many of these patterns can be explained with an analytic model based on constrained and unconstrained sections of the genome. We postulate that the phenotype bias towards simplicity and other patterns biomorphs share with molecular genotype-phenotype maps may hold more widely for developmental systems.Author summary: The question of how novel phenotypic variation arises has received much less attention than natural selection even though both are key processes in Darwinian evolution. Here we uncover striking anisotropic structure in phenotypic variation for biomorphs, Richard Dawkins’s iconic schematic model of development, introduced in his book The Blind Watchmaker. We observe strong simplicity bias: upon uniform random sampling of genotypes, a simple biomorph can be exponentially more likely to appear as potential variation than any individual complex biomorph is. The mapping from genotypes to phenotypes (GP map) for biomorphs exhibits many similarities to molecular GP maps, including relatively high mutational phenotype robustness which is positively correlated with evolvability. Such structure in the arrival of variation can enhance the ability of evolution to find fitness maxima through neutral exploration. By using evolutionary simulations, we show that phenotypes that fix in a population may not be the fittest ones, but rather adaptive phenotypes that are most likely to appear as variation. We hypothesize that similar developmental bias as observed in the biomorphs system may occur more widely in developmental systems.