Significance: Phylogenies are the basis of many ecological and evolutionary studies. However, zokor phylogeny and speciation patterns are heavily debated. This study disentangled the phylogeny and speciation of zokors genomically. Six species of the Eospalax were separated into high-altitude E. baileyi and E. smithi and the rest four low-altitude species by recent Qinghai-Tibet Plateau uplift 3.6 million y ago. E. rothschildi and E. smithi speciated south of the Qinling–Huaihe Line, where refuges were supplied during glaciation. Introgression and incomplete lineage sorting led to the complex phylogeny of zokors. Genomic islands were formed due to ancient polymorphisms and divergence hitchhiking. This study concluded that climatic, geological, and tectonic events shaped the phylogeny and speciation of zokors in China.

Significance: We substantiate genomically, repeatomically, and epigenomically the origin, demography, and timing of two divergent speciation models in the Israeli five blind subterranean species ofSpalax ehrenbergisuperspecies. Four species demonstrate a regional, chromosomal, peripatric, climatic aridity speciation model trending southward from the northern cold and humid Golan and Upper Galilee to the hot, dry Negev Desert. The fifth species shows a local, genic, geologic-edaphic, and sympatric speciation model demonstrating primary sympatric speciation in subterranean mammals. The five species are differentiated at multiple genomic levels and demonstrate different ecological mechanisms of speciation in the superspecies. Sympatric speciation may be common in nature. Numerous ecologically divergent microsites—geologic, edaphic, climatic, abiotic, biotic—abound globally, where selection overrules gene flow homogenization.

Significance: Whether sympatric speciation (SS) is rare or common is still debated. Two populations of the spiny mouse,Acomys cahirinus, from Evolution Canyon I (EC I) in Israel have been depicted earlier as speciating sympatrically by molecular markers and transcriptome. Here, we investigated SS both genomically and methylomically, demonstrating that the opposite populations of spiny mice are sister taxa and split from the common ancestor around 20,000 years ago without an allopatric history. Mate choice, olfactory receptors, and speciation genes contributed to prezygotic/postzygotic reproductive isolation. The two populations showed different methylation patterns, facilitating adaptation to their local environment. They cope with abiotic and biotic stresses, due to high solar interslope radiation differences. We conclude that our new genomic and methylomic data substantiated SS.

The gut microbiome is important for host nutrient metabolism and ecological adaptation. However, how the gut microbiome is affected by host phylogeny, ecology and diet during sympatric speciation remain unclear. Here, we compare and contrast the gut microbiome of two sympatric blind mole rat species and correlate them with their corresponding host phylogeny, ecology soil metagenomes, and diet to determine how these factors may influence their gut microbiome. Our results indicate that within the host microbiome there is no significant difference in community composition, but the functions between the two sympatric species populations vary significantly. No significant correlations were found between the gut microbiome differentiation and their corresponding ecological soil metagenomes and host phylogeny. Functional enrichment analysis suggests that the host diets may account for the functional divergence of the gut microbiome. Our results will help us understand how the gut microbiome changes with corresponding ecological dietary factors in sympatric speciation of blind subterranean mole rats.

Soil bacteria respond rapidly to changes in new environmental conditions. For adaptation to the new environment, they could mutate their genome, which impacts the alternation of the functional and regulatory landscape. Sometimes, these genetic and ecological changes may drive the bacterial evolution and sympatric speciation. Although sympatric speciation has been controversial since Darwin suggested it in 1859, there are several strong theoretical or empirical evidences to support it. Sympatric speciation associated with soil bacteria remains largely unexplored. Here, we provide potential evidence of sympatric speciation of soil bacteria by comparison of metagenomics from two sharply contrasting abutting divergence rock and soil types (Senonian chalk and its rendzina soil, and abutting Pleistocene basalt rock and basalt soil). We identified several bacterial species with significant genetic differences in the same species between the two soil types and ecologies. We show that the bacterial community composition has significantly diverged between the two soils; correspondingly, their functions were differentiated in order to adapt to the local ecological stresses. The ecologies, such as water availability and pH value, shaped the adaptation and speciation of soil bacteria revealed by the clear-cut genetic divergence. Furthermore, by a novel analysis scheme of riboswitches, we highlight significant differences in structured non-coding RNAs between the soil bacteria from two divergence soil types, which could be an important driver for functional adaptation. Our study provides new insight into the evolutionary divergence and incipient sympatric speciation of soil bacteria under microclimatic ecological differences.