Speciation mechanisms and species identification remain controversial. Two different  speciation models occur in Israeli subterranean mole rats, genus Spalax. A regional speciation cline southward of four peripatric, climatic, chromosomal species, and a local, edaphic, genic and sympatric speciation. Here, we highlighted their genome evolution. The five species (Figs. 1-5), evolving in the Pleistocene, from 1.3-1.6 million years ago,  separated into five genetic clusters by SNPs, CNVs, repeatome, and methylome in sympatry, demonstrating that both the coding and noncoding genome regions are subjected to the same climatic ecological stresses and selection, in the four chromosomal species, forming a southward speciation trend, correlated regionally  with increasing aridity. They involve from north to south: Spalax galili (2n= 52), S. golani (2n=54), S. carmeli (2n= 58), and S. judaei (2n= 60) sibling species, un-distigushable phenotypically (Fig. 1). The regional interspecific divergences correspond to Pleistocene climatic cycles. Climate warmings caused chromosomal speciation. Triple effective size populations (Ne) declines match glacial cold cycles (Fig. 2). Adaptive genes and regulation evolved under positive selection to underground stresses, and divergent climates, involving species-specific vocal dialects, and species specific seismic communication (head thumping onto the ceiling). Both cause pre-mating behavioral reproductive isolation.

Meiotic disturbances cause post-mating  reproductive isolation in the four chromosomal species.

Species population demography , and genome divergence between sympatric and peripatric species appear in Figs. 3 and 4, Respectively. Genetic relationships of genomic islands evolved mainly due to adaptive evolution involving ancient polymorphisms (Fig. 5). Repeatome, including copy number variation (CNV), separated N-S species pairs, sympatric species, and identified L1 repetitive elements and mitochondrial genes (Fig. 6) . Methylation in sympatry due to geologic-edaphic abutting divergence (Figs. 1, 5), identified chalk-basaltspecies, differentially affecting thermoregulation, hypoxia, DNA repair, P53 and other pathways. Genome adaptive evolution highlights climatic and edaphic ecologic-tress evolution, and the two speciation models, peripatric and sympatric. Spalax is known to speciate chromosomally. Here we demonstrate the first sympatric speciation in Spalax, and apparently in subterranean mammals. Sympatric speciation may be common in nature, with gene flow, in microsites divergent climatically, geologically, edaphically, biotically and abiotically, as first hypothesized by Darwin, and proved as hot spots in the Evolution Canyon and Evolution Plateau in Israel.

Fig. 1 The ecogeographic distribution and the genomic divergence among Spalax species in Israel

Fig. 2 Genetic relationships between and within species.

Fig. 3 Population demography of five Spalax species based on whole genome re-sequencing data.

Fig. 4 Genome divergence between the sympatric and peripatric species.

Fig. 5 Gene ontology (GO) of genes within islands and differential methylated regions.

This project was supported by the National Natural Science Foundation of China (32071487), Lanzhou University’s “Double First-Class” Guided Project Team Building-Funding-Research Startup Fee (K.L.), the Chang Jiang Scholars Program, the International Collaboration 111 Programme (BP0719040), and the Ancell–Teicher Research Foundation for Genetic and Molecular Evolution.

Fig. 6. Copy number variation and retrotransposon LINE1 of the Spalax ehrenbergi superspecies.

Link: https://www.pnas.org/content/pnas/early/2020/12/03/2018123117.full.pdf