Selection of p53 pathway in adaptive evolution and reproductive isolation in incipient sympatric speciation of Drosophila at Evolution Canyon

Sympatric speciation (SS) refers to the origin of new species within a freely breeding population. The ‘Evolution Canyon’ (EC) in Israel is a natural microsite model for SS of species across phylogenies from viruses and bacteria to mammals, adapting to, and speciating in, interslope microclimates. The cosmopolitan Drosophila melanogaster at EC I, Mount Carmel, is undergoing incipient SS in response to sharply divergent interslope microclimate stresses, including solar radiation, temperature, humidity and pathogenicity. We demonstrated here a selective interslope divergence of single nucleotide polymorphism (SNP) distribution in the Drosophila p53 pathway. This involves a total of 71 genes, which are associated with DNA repair, heat response, and fungal and bacterial resistant pathways. This distribution pattern links the previously observed thermotolerance and ageing divergence of D. melanogaster between the opposite canyon slopes: the south-facing slope (SFS, or African slope: tropical, savannoid and dry) and the abutting north-facing slope (NFS, or European slope; temperate, forested, cool and humid). The genes with interslope-significant differential SNPs link the p53 pathway with pathways related to the responses to microclimates through protein-protein interaction. Moreover, for the first time we provide evidence that the p53 pathway is linked to reproductive isolation, and is thus actively participating in incipient SS of D. melanogaster. This is the first demonstration of a link between the p53 pathway and reproductive isolation, thereby contributing to adaptive incipient sympatric speciation.