Exceptional Chromosomal Evolution and Cryptic Speciation of Blind Mole Rats Nannospalax Leucodon (Spalacinae, Rodentia) from South-Eastern Europe
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G C A T T A C G G C A T genes Review Exceptional Chromosomal Evolution and Cryptic Speciation of Blind Mole Rats Nannospalax leucodon (Spalacinae, Rodentia) from South-Eastern Europe Ivo Savi´c 1, Duško Cirovi´c´ 1 and Vanja Bugarski-Stanojevi´c 2,* ID 1 Biological Faculty, University of Belgrade, 11000 Belgrade, Serbia; [email protected] (I.S.); [email protected] (D.C.)´ 2 Institute for Biological Research “Siniša Stankovi´c“,University of Belgrade, 11060 Belgrade, Serbia * Correspondence: [email protected]; Tel.: +381-11-207-8331 Received: 30 August 2017; Accepted: 17 October 2017; Published: 25 October 2017 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. Keywords: karyotype evolution; chromosomal rearrangements; speciation; cryptic species; cytotypes; chromosomal forms; fossorial; underground 1. Introduction With more than 2000 described species, rodents are the most abundant mammalian order, with 42% of its total species diversity [1]. Molecular phylogenetics and cytogenetics has enabled continuous growth in the number of newly discovered species, often revealing morphologically similar but genetically and/or karyotypically divergent cryptic species [2]. Chromosomal rearrangements (CRs) are frequent among rodents, especially in the two most species-rich families, Cricetidae and Muridae [3]. However, there is no default rate of karyotype evolution. While considerable chromosomal conservation was found in certain taxa (castorimorph and anomaluromorph rodents), some karyotypes of the myomorphs were highly reorganized [4–9]. Similarly, two genera of the Eurasian blind mole rat (BMRs), subfamily Spalacinae (Gray, 1821) ([1,10–15] and others): the greater BMR genus Spalax (Guldenstaedt, 1770) and the lesser BMR genus Nannospalax (Palmer 1903), have opposed rates of the karyotype change, i.e., highly conserved chromosomes and extensive karyotype variability, respectively. Nowadays many studies reach beyond standard research models, such as the mouse (Mus) and the rat (Rattus), in order to trace the evolution of crucial characters. Distinctive in many ways, BMRs have become a valuable research object, particularly because of their remarkable resistance to cancer and their longevity [16–20], besides other distinguishing features. These include tolerance to hypercapnia Genes 2017, 8, 292; doi:10.3390/genes8110292 www.mdpi.com/journal/genes Genes 2017, 8, 292 2 of 22 Genes 2017, 8, 292 2 of 22 andbesides hypoxia other [20 distinguishing–24], a specific features. lipid profile These includ [25] splicee tolerance variants to hypercapnia of heparanase and unique hypoxia in [20–24], mammals, a asspecific well as lipid particular profile expression [25] splice patterns variants for of p53heparanase [26,27], circadianunique in rhythms mammals, [28 ]as sensory well as research particular [21 ]. Inexpression addition, cytogeneticpatterns for analysis p53 [26,27], has revealed circadian a distinguishing rhythms [28] karyotypesensory research evolution [21]. [11 ,29In –addition,31]. cytogeneticEven though analysis they has are revealed appreciated a distin asguishing a research karyotype object, BMRsevolution are seriously[11,29–31]. endangered in their naturalEven habitat, though primarily they are because appreciated of an inappropriate as a research conservationobject, BMRs status, are seriously resulting endangered from an unresolved in their taxonomynatural habitat, with an primaril unrecognizedy because species of an [1 ].inappropriate In the International conservation Union forstatus, Conservation resulting from of Nature an (IUCN)unresolved Red Listtaxonomy of Threatened with an unrecognized Species [32 ],species only three[1]. In speciesthe International of BMRs Union are acknowledged for Conservation and categorizedof Nature (IUCN) as Data Red Deficient List of (DD). Threatened Many Species populations [32], only and speciesthree species are therefore of BMRs under are acknowledged serious threat, particularlyand categorized due to as the Data loss Deficient and fragmentation (DD). Many of po theirpulations natural and habitats species [ 33are,34 therefore]. under serious threat,Eurasian particularly BMRs aredue typical to the residentsloss and fragme of grassyntation steppes, of their hills, natural and mountain-meadows habitats [33,34]. of the Eastern MediterraneanEurasian region,BMRs are including typical residents Eastern andof grassy South-eastern steppes, hills, Europe, and Western mountain-meadows Asia, and Northern of the AfricaEastern (Figure Mediterranean1). They range region, in altitudeincluding from Easter belown and sea South-eastern level to an elevation Europe, ofWestern 2600 m Asia, above and sea levelNorthern (a.s.l.) Africa [1,35, 36(Figure] and also1). They inhabit range cultivated in altitude areas, from sparsebelow woodlands,sea level to an steppes, elevation and of mountain2600 m slopes,above but sea do level not (a.s.l.) occur in[1,35,36] dense forestsand also and inhabit marshy cultivated areas [10 areas,,13,35 ,sparse37–40]. woodlands, Spalacines aresteppes, herbivores, and mountain slopes, but do not occur in dense forests and marshy areas [10,13,35,37–40]. Spalacines are eating mostly roots, tubers, rhizomes, and a little grass and grain. With subcutaneous vestigial eyes herbivores, eating mostly roots, tubers, rhizomes, and a little grass and grain. With subcutaneous restricted to photoperiod perception, most of their lifetime is confined to underground tunnels [35]. vestigial eyes restricted to photoperiod perception, most of their lifetime is confined to underground They are chisel-tooth diggers, using their lower incisors for burrowing and the lower jaw as a shovel. tunnels [35]. They are chisel-tooth diggers, using their lower incisors for burrowing and the lower Due to solitary, territorial, and aggressive behavior, their distribution is additionally fragmented [40]. jaw as a shovel. Due to solitary, territorial, and aggressive behavior, their distribution is additionally The many adaptations necessary for living underground in cylindrical tunnels have defined their fragmented [40]. The many adaptations necessary for living underground in cylindrical tunnels have phenotypedefined their and obscuredphenotype their and actual obscured phylogenetic their actu relations.al phylogenetic Thus, convergent relations. morphology Thus, convergent on the one handmorphology and the intensive on the one chromosomal hand and the speciationintensive chromosomal on the other speciation tangle Spalacinae on the othersystematics tangle Spalacinae and divide taxonomistssystematics since and divide they were taxonomists first discovered. since they were first discovered. FigureFigure 1. 1.Geographic Geographic distribution distribution of Nannospalaxof Nannospalax leucodon leucodonchromosomal chromosomal forms forms (CF) (CF) from from South-eastern South- Europeeastern (reproduced Europe (reproduced with permission with permission from [29 ],from Figure [29], 2,Figure adapted). 2, adapted). Red—the Red—the Yugoslav Yugoslav branch; yellow—thebranch; yellow—the Serbicus branch; Serbicus blue–the branch; North blue–the Balkan Nort subsidiaryh Balkan branch; subsidiary violet–the branch; South violet–the Balkan subsidiary South Balkan subsidiary branch; green—the East Balkan branch. Small map: N. leucodon distribution area branch; green—the East Balkan branch. Small map: N. leucodon distribution area from International Union from International Union for Conservation of Nature (IUCN) Red List of Threatened Species. For for Conservation of Nature (IUCN) Red List of Threatened Species. For symbols see Table1. symbols see Table 1. Genes 2017, 8, 292 3 of 22 Table 1. Chromosomal forms (CFs) and localities of recent and extinct Nannospalax leucodon from South-eastern Europe, as presented in Figure1:( a) CFs grouped in four branches, following [29]; (b) fossil findings with localities. (a) CF 2n NF Sampling Localities Branches [29] Tara, Zlatibor, Cajetina,ˇ Cigota,ˇ Kopaonik, Vlasina-Klisura, 1 montanoserbicus 56 82 Vlasina-Sokolovo, Cakor.ˇ I 2 hercegovinensis 54 90 Durmitor, Zelengora, Magli´c, Cemerno,ˇ Neretva, Gvozd, Njegovuđa. Višnjica, B. brdo, Košutnjak, Avala, Jajinci, Smederevo-Udovice, 3 syrmiensis 54 90 Bogati´c(Maˇcva),St. Pazova. 4 hungaricus 48 84 Hajdukovo, Šušara,