System drift and speciation

Even if a species’ phenotype does not change over evolutionary time, the underlying mechanism may change, as distinct molecular pathways can realize identical phenotypes. Here we use quantitative genetics and linear system theory to study how a gene network underlying a conserved phenotype evolves, as the genetic drift of small changes to these molecular pathways cause a population to explore the set of mechanisms with identical phenotypes. To do this, we model an organism’s internal state as a linear system of differential equations for which the environment provides input and the phenotype is the output, in which context there exists an exact characterization of the set of all mechanisms that give the same input–output relationship. This characterization implies that selectively neutral directions in genotype space should be common and that the evolutionary exploration of these distinct but equivalent mechanisms can lead to the reproductive incompatibility of independently evolving populations. This evolutionary exploration, or system drift, proceeds at a rate proportional to the amount of intrapopulation genetic variation divided by the effective population size (Ne). At biologically reasonable parameter values this process can lead to substantial interpopulation incompatibility, and thus speciation, in fewer than Ne generations. This model also naturally predicts Haldane’s rule, thus providing another possible explanation of why heterogametic hybrids tend to be disrupted more often than homogametes during the early stages of speciation.