Exceptional Chromosomal Evolution and Cryptic Speciation of Blind Mole Rats Nannospalax leucodon (Spalacinae, Rodentia) from South-Eastern Europe

Abstract

Mole rats are exclusively subterranean and highly specialized rodents. Their long lifespans, remarkable anti-cancer mechanisms, and various distinctive adaptive features make them a useful research model. Moreover, opposing convergence of morphological traits, they have developed extremely high karyotype variability. Thus, 74 chromosomal forms have been described so far and new ones are being revealed continuously. These evolved during the process of rapid radiation and occur in different biogeographical regions. During research into their reproductive biology we have already provided substantial evidence for species-level separation of these taxa. Here, we review diverse chromosomal forms of the lesser blind mole rat, Mediterranean Nannospalax leucodon, distributed in South-eastern Europe, their karyotype records, biogeography, origin, and phylogeny from our extensive research. In the light of new data from molecular genetic studies, we question some former valuations and propose a cryptospecies rank for seven reproductively isolated chromosomal forms with sympatric and parapatric distribution and clear ecogeographical discrepances in their habitats, as well as new experimental and theoretical methods for understanding the courses of speciation of these unique fossorial mammals.

Phylogeny and biogeography of the African Bathyergidae: a review of patterns and processes

“…Adaptive differences (ecological, physiological, behavioral, morphological and genetic) in the fossorial genus Spalax have been intensively studied over the past three decades in four parapatric chromosomal species distributed across an ecogeographical and climatic gradient in Israel (Nevo & Bar-El, 1976; Nevo, 1985; Nevo et al, 1994, 2000). To some extent, similar patterns have been demonstrated in the fossorial genera Nanospalax (Savić, Ćirović & Bugarski-Stanojević, 2017) and Geomys (Heaney & Timm, 1985). Based on advances in genomic sequencing abilities, more recent studies have successfully employed data on adaptive genes and gene expression (whole mitochondrial and nuclear DNA genomes, transcriptomes, DNA methylation, micro RNA and codon usage) to show adaptive ecological speciation between two Spalax species which inhabit adjacent areas contrasting sharply in geology, edaphic attributes, vegetation and ecology (Hadid et al, 2012; Lövy et al, 2015; Li et al, 2015, 2016; Zhao et al, 2016).…”

Multi-Locus Genetic Identification of a Newly Discovered Population Reveals a Deep Genetic Divergence in European Blind Mole Rats (Rodentia: Spalacidae: Nannospalax)

“…Species of Spalacinae can hardly cross large rivers, therefore, such a barrier can easily trigger allopatric divergence (Pyron & Burbrink 2010); moreover, all taxa with unique chromosomal arrangement investigated so far are known to be reproductively isolated from the neighbouring taxa (Savić & Soldatović 1984, Savić et al 2017. Geographic barriers, especially large rivers are known to be effective barriers for animal species with a reduced mobility and can have an isolating effect on populations (e.g., Trizio et al 2005, Kennis et al 2011 and species (e.g.…”

“…From the grasslands of the Pannonian (or Carpathian) Basin four Nannospalax taxa have been described: N. (leucodon) transsylvanicus Méhely, 1909; N. (leucodon) hungaricus Nehring, 1898; the most likely extinct N. (leucodon) syrmiensis Méhely, 1909 and N. (leucodon) montanosyrmiensis Savić and Soldatović, 1974(Savić and Soldatović 1984, Csorba et al 2015. The latter taxon (the Vojvodina blind mole rat) was originally described on karyological grounds by Savić and Soldatović (1974) as Spalax montanosyrmiensis from two neighbouring localities (Stražilovo and Čortanovci) on the Fruška gora in Vojvodina, Serbia, and proved to be reproductively isolated from other chromosomal forms of Nannospalax in the region (Savić & Soldatović 1984, Savić et al 2017. During the research of blind mole rats of the Pannonian Basin, a small and fragmented population of blind mole rats was found in 2008 between Subotica (N Serbia) and Kelebia (S Hungary) (Németh et al 2013a).…”

“…The lesser blind mole rat Nannospalax leucodon Nordmann, 1840 superspecies is endemic to Europe and characterised by high chromosomal diversity (Kryštufek & Vohralík 2009), with 25 karyologically distinct forms reported so far (see Arslan et al 2016). Although the species status of taxa described in the genus solely on chromosomal grounds has not been widely accepted (Kryštufek 1997, Kryštufek et al 2012, breeding experiments on several chromosomal forms (Savić & Soldatović 1984, Savić et al 2017, corroborated by the results of recent molecular phylogenetic investigations (Hadid et al 2012, Kryštufek et al 2012, Németh et al 2013a, strongly suggest the possibility of the existence of cryptic species status of some of these forms.…”

A Cryptic Subterranean Mammal Species, the Lesser Blind Mole Rat (Nannospalax leucodon syrmiensis)—Retreated but Not Extinct

“…These vastly unusual rodents are represented by two genera: the greater BMR, Spalax (Guldenstaedt 1770), and the lesser BMR, Nannospalax (Palmer 1903). The latter represents an excellent research model for chromosomal speciation studies, as the genus Nannospalax includes 74 groups with fixed chromosomal differences [ 6 , 7 , 8 ] with a wide range of diploid chromosomal number (2 n ), from 36 to 60. These chromosomal forms (CFs) are alternatively labelled as cytotypes, races, or sibling/good biological/cryptic species [ 8 , 9 , 10 ].…”