Transcriptome, genetic editing, and microRNA divergence substantiate sympatric speciation of blind mole rat, Spalax

Abstract

Incipient sympatric speciation in blind mole rat, Spalax galili, in Israel, caused by sharp ecological divergence of abutting chalkbasalt ecologies, has been proposed previously based on mitochondrial and whole-genome nuclear DNA. Here, we present new evidence, including transcriptome, DNA editing, microRNA, and codon usage, substantiating earlier evidence for adaptive divergence in the abutting chalk and basalt populations. Genetic divergence, based on the previous and new evidence, is ongoing despite restricted gene flow between the two populations. The principal component analysis, neighbor-joining tree, and genetic structure analysis of the transcriptome clearly show the clustered divergent two mole rat populations. Gene-expression level analysis indicates that the population transcriptome divergence is displayed not only by soil divergence but also by sex. Gene ontology enrichment of the differentially expressed genes from the two abutting soil populations highlights reproductive isolation. Alternative splicing variation of the two abutting soil populations displays two distinct splicing patterns. L-shaped F ST distribution indicates that the two populations have undergone divergence with gene flow. Transcriptome divergent genes highlight neurogenetics and nutrition characterizing the chalk population, and energetics, metabolism, musculature, and sensory perception characterizing the abutting basalt population. Remarkably, microRNAs also display divergence between the two populations. The GC content is significantly higher in chalk than in basalt, and stress-response genes mostly prefer nonoptimal codons. The multiple lines of evidence of ecologicalgenomic and genetic divergence highlight that natural selection overrules the gene flow between the two abutting populations, substantiating the sharp ecological chalk-basalt divergence driving sympatric speciation.natural selection | ecological adaptive speciation | DNA editing | microRNA regulation | nonoptimal codon usage

Living Organisms Author Their Read-Write Genomes in Evolution

“…As we might expect, the microRNA repertoire of each species is taxonomically specific [ 538 , 539 , 540 ], and thus is a key product of evolutionary variation [ 541 , 542 , 543 ]. A significant role for miRNAs was recently reported in sympatric evolution of naked mole rats [ 544 ]. Mobile and repetitive DNA elements encode or have contributed to the evolution of microRNAs in many different species [ 545 , 546 , 547 , 548 ].…”

Can the environment influence species home‐range size? A case study onCtenomys minutus(Rodentia, Ctenomyidae)

“…Consequently, behavioral changes associated with habitat features may lead to a profound differentiation of aspects related to genetics, morphology and physiology of a species, as was demonstrated for other subterranean rodents such as Spalax galili (Polyakov et al ., ; Hadid et al ., ; Li et al . ; Lövy et al ., ; Šklíba et al ., ), Spalax ehrenbergi (Heth, ) and C. mendocinus (Rosi et al ., ). Future studies including estimates of features associated with home range behavior in this species would be particularly informative.…”

Adaptive evolution of coagulation and blood properties in hypoxia tolerantSpalaxin Israel

“…One population was studied from each Spalax species (see M&M), with an exception in Spalax galili , where two populations have been studied, Dalton and Kerem Ben Zimra, but their results were reported as one population, whereas, recently, the basalt population proved a new sympatric species (Hadid et al ., ; Li et al ., , ; Lövy et al ., ; Šklíba et al ., ). Among the populations reported in this study, Spalax galili , Dalton population, possesses the shortest bleeding time and APTT, and the lowest platelet counts between the populations from the four Israeli Spalax species studied.…”

“…The shorter bleeding time and APTT in Spalax galili (Dalton population) may be an evolutionary adaptation to reduce bleeding after fighting (Nevo, Heth & Beiles, ), due to high population density (Hadid et al ., ; Li et al ., , ; Lövy et al ., ; Šklíba et al ., ) or basalt rock (Hadid et al ., ; Li et al ., ) injuries, and possibly due to the environmental temperature, as it ranges in colder areas compared to other Spalax species, and the basalt soil is colder, than that of the neighboring Kerem Ben Zimra population. Spalax golani Quneitra population might be also at a high risk of injury (though less than the Spalax galili new species in Dalton population) and for bleeding because of the high aggression (Nevo et al ., ), sharp basalt rock and soil (Hadid et al ., ; Li et al ., , ; Lövy et al ., ; Šklíba et al ., ), and cold climatic regime. However, the bleeding time of the four Spalax species are within the normal range of human (2–9 min) (Maleki et al ., ), mouse) 1.1–4.8 min) (Jirouskova, Shet & Johnson, ) and rat (2.0–3.5 min) (Dejana et al ., ).…”