Sympatric speciation of the spiny mouse from Evolution Canyon in Israel substantiated genomically and methylomically

Speciation with ongoing homogenizing gene flow, later dubbed sympatric speciation, has been a fascinating and debated topic since Darwin proposed it. Here, we analyzed sympatric speciation of the spiny mouse, Acomys cahirinus, from Evolution Canyon I, Mount Carmel, Israel, revealed by whole-genome, methylome, and behavior comparisons. Mitochondrial phylogeny indicated that the tropical African Slope (AS) and temperate European Slope (ES) populations were sister taxa and shared a common ancestor. Based on the de novo chromosomal-level genome, we compared the genome and methylome of the two populations from EC I. We found clear-cut divergences between them based on both single nucleotide polymorphisms (SNPs) and structure variations (SVs). We identified 440 highly diverged regions and found olfactory receptors significantly divergent between slopes, suggesting prezygotic reproductive isolation. Furthermore, genes related to adaptation were enriched in immunity, temperature homeostasis in AS and energy, and cell cycle in ES. Population demographic modeling showed that the AS and ES populations split from the same ancestor with decreasing gene flow, implying sympatric speciation. Epigenetic methylation divergence preceded genetic differentiation and facilitated slope adaptation and sympatric speciation. We found a significant difference in activity onset in laboratory between the two populations, associated with the methylation divergence of circadian genes. We concluded that behavioral, genomic, and methylomic divergence substantiated sympatric speciation of Acomys from EC I in Israel, shown earlier transcriptomically.