Reproductive barriers as a byproduct of gene network evolution

Molecular analyses of closely related taxa have increasingly revealed the importance of higher-order genetic interactions in explaining the observed pattern of reproductive isolation between populations. Indeed, both empirical and theoretical studies have linked the process of speciation to complex genetic interactions. Gene Regulatory Networks (GRNs) capture the inter-dependencies of gene expression and encode information about an individual’s phenotype and development at the molecular level. As a result, GRNs can–in principle–evolve via natural selection and play a role in non-selective, evolutionary forces. Here, we develop a network-based model, termed the pathway framework, that considers GRNs as a functional representation of coding sequences. We then simulated the dynamics of GRNs using a simple model that included natural selection, genetic drift, and sexual reproduction and found that reproductive barriers can develop rapidly between allopatric populations experiencing identical selection pressure. Further, we show that alleles involved in reproductive isolation can predate the allopatric separation of populations and that the number of interacting loci involved in genetic incompatibilities, i.e., the order, is often high simply as a by-product of the networked structure of GRNs. Finally, we discuss how results from the pathway framework are consistent with observed empirical patterns for genes putatively involved in post-zygotic isolation. Taken together, this study adds support for the central role of gene networks in speciation and in evolution more broadly.