Genomic and epigenomic analyses reveal speciation in mole rat populations without sharp separation
For new species to evolve, conventional wisdom suggests that geographically isolated populations must exist that form separate reproductive communities. This isolation allows the genomes to slowly diverge and thus form new species. An international research team with participation of the Leibniz Institute for Zoo and Wildlife Research (Leibniz-IZW) and the University of Haifa has now reconstructed the first reported case of local speciation within a common gene pool in subterranean mole rats, a group of species which are rodents.
Four out of five mole rat species of the superspecies Spalax ehrenbergi originated due to climate divergence over the past 1.5 million years, regionally across the country, and locally in the Upper Galilee through geological and soil microscale adaptive divergence in the last 228,000 years without chromosomal divergence in a common region. The latter local mechanism is called "sympatric speciation" and has now been demonstrated for the first time in a subterranean mammal in the team's paper published in the “Proceedings of the National Academy of Sciences of the United States of America”.
Even more than 160 years after the publication of Charles Darwin's “On the Origin of Species”, the mechanisms of speciation are still not fully understood. For example, it is still controversial whether sympatric speciation is a rare or common mechanism driving the evolution of new wildlife species. In order to better understand modes of speciation with small populations without spatial segregation, scientists from the University of Haifa, together with international colleagues, analysed the genome of the five species of blind subterranean mole rats (family Spalacidae) living in Israel. Four of the five species speciated chromosomally (diploid chromosomes = 52, 54, 58, and 60) and can be assigned to separate ranges adjacent to each other from northern humid to dry southern Israel. This spatial distribution coincided with Pleistocene climatic cycles: A warming of the regional climate between ice ages was responsible for a diversification of the chromosome number of the four species. This speciation mechanism, which occurs in spatially segregated areas through evolutionary adaptations to local environmental conditions in the periphery of the ancestral species is called “peripatric” speciation. In the case of the four Spalax species, the distribution areas were only slightly isolated in the periphery of the ancestral species rather than in a geographically distant region from the ancestor, a mechanism called “allopatric speciation”. Nevertheless, the new peripatrically emerging species evolved reproductive isolation, which supported speciation. In detail the Spalax species developed different communication dialects and different vibrations called “seismic” or “vibratory” communications, both behaviours are regarded as “pre-mating reproductive isolation”. Additionally, they also evolved chromosomal incompatibilities, called “post-mating reproductive isolation”, thereby generating new biological species, with narrow hybrid zones separating the four species.
“One of the major aims of our study was clearly to show that even in Spalax, which usually speciates chromosomally, sympatric speciation occurred between the ancestor chalk species, and the new sympatric species on the basalt in Upper Galilee at Evolution Plateau. All five Spalax species can be identified by single-nucleotide polymorphisms (SNPs), coexistence of copy number variations (CNVs), repeatome and methylome. The importance of this is the fact that even after some 160 years from the time Darwin hypothesised it, a major ongoing debate in evolutionary biology is the frequency of sympatric speciation in nature. Most biologists think it is rare in nature whereas all our speciation studies at the Evolution Canyon and Evolution Plateau models indicates the opposite: The “sympatric speciation model” may be a common speciation model because millions of Evolution Canyons exist in our planet based on microsites with divergent ecologies, geological, edaphic, climatic, abiotic and biotic, in canyons or on plateaus, and slope topographies. Hence “sympatric speciation” must be a common model in nature across life from viruses and bacteria through fungi, plants, and animals, here demonstrated by the non-chromosomal new basalt sympatric species, in the northern species complex of Spalax galili,” explains Prof Eviatar Nevo from the University of Haifa.
In the north of Israel, the scientific team characterised two species which shared their range: Spalax galili comprises two distinct species that adapted to small-scale divergence in local geological and edaphic abutting conditions in the same area. SNPs, CNVs, repeatome and methylome results support each other. “Spalax galili chalk and Spalax galili basalt differed significantly in their methylation patterns,” explains Dr Alexandra Weyrich from the Leibniz-IZW, who was responsible for the analyses of the so-called epigenome.
The epigenome can be referred to as an “instruction manual for genes” in that it determines which genes of the genome are activated and thus sets the properties of cells and organs. “As the names of the two species already suggest, these epigenetic differences are related to the local rock in which the animals live, chalk and basalt, sedimentary and igneous rocks, respectively. We were able to identify genes with differently methylated regions (DMRs) between the two species, which are relevant for heat regulation and oxidative stress, among other functions,” says Weyrich. This indicates that within a species range speciation and local adaptive rock/soil divergence at the microsites, sharply divergent ecologically, took place and thus advanced reproductive isolation between the two groups. The analysis of the genome and the epigenome of the Israeli mole rats therefore demonstrated for the first time in a subterranean mammal speciation with selection overriding gene flow homogenisation, which might be a frequent event across life from viruses and bacteria to mammals. Sympatric speciation was first hypothesised by Charles Darwin and demonstrated in Israel both at the “Evolution Canyon Microclimatic Model”, and in the “Evolution Plateau Geological-edaphic Model” by abutting divergent ecologies in blind subterranean mammals, which speciated sympatrically and non-chromosomally. Thus, there are multiple speciation models dependent on ecological divergence.
Dr Alexandra Weyrich
Scientist in the Department of Evolutionary Genetics
Leibniz Institute for Zoo and Wildlife Research (Leibniz-IZW)
in the Forschungsverbund Berlin e.V.
Alfred-Kowalke-Str. 17, 10315 Berlin
phone: +49 (0)30 5168313
LI K, Zhang S, Song X, Weyrich A, Wang Y, Liu X, Wan N, Liu J, Lövy M, Cui H, Frenkel V, Titievsky A, Panov J, Brodsky L, Nevo E (2020): Genome evolution of blind subterranean mole rats: Adaptive peripatric and sympatric speciation. PNAS 117, 32499-32508; https://doi.org/10.1073/pnas.2018123117.