Pairwise Hybrid Incompatibilities Dominate During Allopatric Speciation For A Simple Genotype-Phenotype Map Of Embryonic Spatial Patterning

Understanding the origin of species is as Darwin called it “that mystery of mysteries”. Yet still, how the processes of evolution give rise to non-interbreeding species is not well understood. In an empirical search for a genetic basis, transcription factor DNA binding has commonly been identified as being an important factor in the development of reproductive isolation. This is supported by computational and theoretical models based on the biophysics of transcription factor DNA binding that provide a mechanistic basis of such incompatibilities between allopatrically evolving populations. However, gene transcription mediated by such binding events occurs within the context of larger gene regulatory networks, so the question remains how important are such pair-wise interactions compared to higher order interactions in determining incompatibilities. Orr calculated that as the order of interaction increases there are more pathways for an incompatibility to occur. Here, we show, using simulations based on a simple biophysical genotype phenotype map of spatial patterning in development, that biophysics provides a stronger constraint, leading to pair-wise incompatibilities arising more quickly and being more numerous than higher order incompatibilities, when there is stabilising selection on each allopatric lineage. In addition, we show that incompatibilities arise more quickly for smaller populations and in a manner supporting previous conclusions from models of hybrid incompatibility based solely on transcription factor DNA binding.