We explore how the genotype-phenotype map determines convergent evolution in a simple model of spatial gene regulation during development. Evolution is simulated via a Monte Carlo scheme that incorporates mutation, selection, and genetic drift, by using a bottom-up model of gene regulation with a fitness function that is optimized by a switch-like response to a morphogen gradient. We find that even for very simple regulation, the genotype-phenotype map gives rise to an emergent fitness landscape of remarkable complexity. This leads to a richness of evolutionary behavior as population size is increased that parallels the thermodynamics of physical systems as temperature decreases. Convergence is controlled by the existence of sufficiently dominant global optima in ''free fitness,'' which is a quantity that is the balance of mutational entropy and fitness. In independent simulations at low population sizes, we find convergence to a phenotype of suboptimal fitness due to the multiplicity or entropy of solutions. This contrasts with convergence to the optimal fitness phenotype at high population size. However, at sufficiently large population sizes, we find convergence in only the phenotypes with greatest effect on fitness, whereas noncritical phenotypes exhibit divergence due to quenched disorder on a locally rough landscape. Our results predict that for large populations, the evolution of even simple gene regulatory circuits may be glassy-like, such that, counter to the commonly accepted view that conservation implies function, many conserved phenotypes are simply frozen accidents of little consequence to the fitness of the organism.fitness landscapes ͉ gene regulation ͉ genotype-phenotype map ͉ mutational entropy ͉ population genetics O ver the past 150 years, much work has established natural selection, mutation, and genetic drift as the basic processes of evolution (1-5). However, there still remains much controversy concerning how the complexity and diversity of biological form has arisen from essentially random processes; does evolution play out in an arena of weak constraints, or are there hidden limits to the possibilities of biological form. This is epitomized in the debate regarding the role of historical contingency in evolution; were we to replay the tape of life, would, as Stephen Jay Gould (6) suggested, historical accidents compound and amplify in time such that biological organisms on Earth today would be unrecognizable, or is evolution constrained to the extent that life forms would correspond with those on earth today, as argued by Simon Conway Morris (7). There are many examples in the natural world of independent convergence that support the latter stance, a famous example is the near-identical structure of the mammalian and octopus camera eye (7), whereas empirical support for divergence in evolution is rarer, because by its very nature, the demonstration of different solutions under the same selective pressure is difficult. At the heart of this debate is that, despite an understanding of the b...