Spalax Research Articles

Soil preference in blind mole rats in an area of supposed sympatric speciation: do they choose the fertile or the familiar?

AbstractAnimals become adapted to different habitats, which, under some circumstances, may lead to speciation. Such speciation can possibly take place even in sympatry, as has recently been suggested in the blind mole rat Spalax galili surveyed at a microsite where two soil types of ecologically contrasting characteristics, basaltic soil and rendzina soil, abut each other. Such speciation would be possible if mole rats developed reproductive isolation, for example, by means of habitat choice. In our study, we quantified food supply and soil characteristics of 20 blind mole rat burrow systems in both soils at a new microsite and tested the mole rat's soil preference in a T‐maze. The basaltic soil was harder and heavier than the rendzina soil, and had higher density and biomass of food, which is comparable to the published data from the only other studied microsite 3.7 km apart. Mole rats preferred to burrow in their familiar soil, when the tested soils were moist. After the soils were dried, both groups of mole rats tended to burrow preferentially in the rendzina soil, nevertheless, this preference was only significant in rendzina‐soil mole rats. We propose that after the suppression of olfactory cues mole rats preferred to burrow in soil with lower energetic costs of burrowing. We suggest that soil preference by mole rats is effective mainly in moist soil that releases specific odorous cues, which coincides with mating season and natal dispersal. This preference could also play an important causative role in reproductive isolation of the two blind mole rat populations.

A new chromosomal race (2n=44) of Nannospalax xanthodon from Turkey (Mammalia: Rodentia)

A new karyotype for blind mole rats was recorded in Tunceli province in Eastern Turkey. The karyotype contained 44 chromosomes, including 13 biarmed pairs, 7 acrocentric pairs, and one heteromorphic pair with a submetacentric and an acrocentric homologue in the autosomal complement (FNa=69). The X chromosome was submetacentric and the Y chromosome medium-sized subtelocentric (FN=73). Distinct dark centromeric C-bands were observed on most of the biarmed and three pairs of the acrocentric autosomes. The NORs were detected on short arms of three subtelocentric pairs and one acrocentric pair of autosomes. The diploid number of chromosomes and the karyotype characteristics observed are obviously unique among hitherto studied populations of blind mole rats and the complement can be evaluated as a new chromosome race of Nannospalax xanthodon. The distribution ranges of individual chromosome races of the species recorded in Eastern Anatolia are revised and possible interracial hybridization is discussed in respect of the finding of a new race.

Adaptive evolution of coagulation and blood properties in hypoxia tolerantSpalaxin Israel

AbstractThe subterranean blind mole rat (Spalax) is adapted to underground life stresses genomically, proteomically, and phenomically. It has been studied multidisciplinarily as an evolutionary model, and a potential medical therapy resource. The four parapatric species in Israel, are climatically adapted. Here, we examine coagulation, and blood properties of one population in each of the fourspecies. Our results show thatSpalax galilipossesses the shortest average bleeding time compared to the otherSpalaxspecies (P < 0.04). Likewise,Spalax galilipossesses the shortest average activated partial thromboplastin time. Prothrombin time is 16.34 ± 4.25, 23.3 ± 8.99, 15.71 ± 4.24, and 17.37 ± 6.02 s inSpalax galili,Spalax golani,Spalax carmeliandSpalax judaei, respectively, with significant differences betweenSpalax galiliandSpalax golani, and betweenSpalax golaniandSpalax carmelipopulations (P < 0.05). Blood hemoglobin is higher inSpalax galiliandSpalax golanicompared toSpalax carmeliandSpalax judaeipopulations. Bleeding time, coagulation profiles, and blood properties differ partly between the examined populations. These differences appear adaptive, associated with climatic variation, population density, and the risk of injury during digging, fighting and preying. The population under the highest injury risk displayed the shortest bleeding time.

SOME HISTOLOGICAL STUDIES ON THE DIGESTIVE SYSTEM OF THE SPALAX LEUCODON (LESSER BLIND MOLE RAT) INHABIT THE EGYPTIAN NORTH COAST

THe aim of the present study is to revealed some anatomical and histological structure of the digestive system of the blind mole rat (spalax leucodon Egyptiac us). Nine blind mole rat of both sex were used for this study .the digestive system of the lesser blind mole rat is resemble to that of other rodents except some variations. The lip are very small as a flap of skin .the incisor teeth are long, curved and powerful .the stomach is unilocular compound type. The proventriculus is demarcated from the glandular gastric regions by limiting ridge. The glandular region contains simple tubular gland, that lined by three types of cells: mucous neck cells, parietal cells and chief cells. The outer longitudinal muscle layer of both cecum and colon showed teniae . We can concluded that the digestive system of spalax leucodon egyptiacus is similar to that of other rodents, and observed differences due to adaptation to habitat and their diet.

Underground life is still safest: comments on ‘Danger underground and in the open – predation on blind mole rats (Rodentia, Spalacinae) revisited’

AbstractNémeth et al. (Mammal Review 46, 2016, 204) recently reviewed the relationships between Old World blind mole rats (Spalacidae) and their predators. They concluded that blind mole rats are regularly taken by predators throughout their range, and that predation pressure probably contributed to blind mole rat evolution and underground behaviour. I argue instead that blind mole rats are rare or accidental prey for most predators, and list a number of alternative explanations for cases where a high predation rate was observed. I conclude that no blind mole rat species that has been studied is important prey for any predator species that can encounter it.

A Macro-Anatomical Investigation of the Some Skull Bones of Nehring's Blind Mole Rats (Spalacidae: Nannospalax nehringi).

This study was aimed to demonstrate the specific anatomical features of the skull bones of Nehring's blind mole rats. Eight skulls, belonging to animals of both sexes, were used. The occipital squama contributed to the formation of the caudal portion of the skull roof. The foramen magnum was quite large. The external occipital crest was present only in the males. The parietal bones formed the middle portion of the skull roof together with the well-developed inter-parietal bones. The zygomatic process of the temporal bone formed the zygomatic arch by extending to the temporal process of the zygomatic bone. The zygomatic process of the frontal bone and the frontal process of the zygomatic bone laterally bordered the orbit. There was a single septal process of the nasal bone. Each ramus of the mandibula had four processes. The mandibular ramus had an angular process on its caudal rim, which extended dorsolaterally. The dorsal free end of the mandibular ramus possessed a coronoid process. In the back, there were two other processes, situated medially and laterally. The medially situated process was referred to as a condylar process, and the laterally situated process was referred to as an alveolar process. The alveolar process detected on the mandibular ramus has not been reported in any rodent species, other than those of the family Spalacidae. Blind mole rats can be a real eye-opener for evolutionary science. The burrowing rodents are key to answering a controversial question about how new species arise.

A LATE PLEISTOCENE RODENT FAUNA (MAMMALIA: RODENTIA) FROM HADŽI PRODANOVA CAVE NEAR IVANJICA (WESTERN SERBIA)

Hadži Prodanova Cave in western Serbia is a multilayered site which, in addition to Palaeolithic tools, has yielded a relatively rich fauna of small and large vertebrates. In this paper the rodent fauna from this site is described. In total, 13 species of rodents have been found: Spermophilus cf. citelloides, Sicista subtilis, Mesocricetus newtoni, Arvicola cf. terrestris, Chionomys nivalis, Microtus arvalis/agrestis, Microtus subterraneus, Clethrionomys glareolus, Apodemus sylvaticus, Apodemus cf. uralensis, Spalax sp ., Muscardinus avellanarius . This fauna has a mixed character and includes species of both open and forest habitats, the former being more numerous. According to its overall composition, it is tentatively ascribed to a relatively mild and wet period of the Last Glacial, probably MIS 3.

Mole-rat from Khortytsia in the light of morphological and geographical relations between Spalax zemni and S. microphthalmus

Mole-rat from Khortytsia in the light of morphological and geographical relations between Spalax zemni and S. microphthalmus

Review of chromosome races in blind mole rats (SpalaxandNannospalax)

The blind mole rats (Spalacinae) reveal fascinating chromosomal variation, resulting from complex karyotype re-arrangements. This variation occurs between species, between populations of single species (polytypy) and within populations (polymorphism). This article reviews the current knowledge on blind mole rats' karyotypes and their variation. A special attention is paid to differentiation of the karyotype within a species and the patterns of chromosomal variation, which result in evolution of distinct chromosomal races (cytotypes). The chromosome races are defined as a group of geographically contiguous or recently separated populations which share a similar chromosome complement by descent. The present review indicated the existence of 73 distinct chromosome races recorded in blind mole rats classified within the genus Nannospalax, along with the seven species recognized within the genus Spalax. In total, 12 distinct diploid numbers of chromosomes were reported (2n = 36-62); and variation in chromosome morphologies was observed between populations with the same number of chromosomes (NF = 62-124). The blind mole rats classified in the genus Spalax revealed rather uniform karyotype both between and within the recognized species. Considering the traditional species classified in the Nannospalax genus, 25 races can be distinguished within N. leucodon, 28 races within N. xanthodon and 20 races within N. ehrenbergi. Hybrids between the races are found only exceptionally and they seem to be almost absent in extensive areas (Europe, Turkey). This fact indicates that chromosomal evolution in blind mole rats may be related to speciation processes. The definitive phylogenetic and taxonomic conclusions can be derived only after application of reliable molecular markers and setting of estimates of genetic distances and gene flow between populations.

Genome maintenance and bioenergetics of the long-lived hypoxia-tolerant and cancer-resistant blind mole rat, Spalax: a cross-species analysis of brain transcriptome.

The subterranean blind mole rat, Spalax, experiences acute hypoxia-reoxygenation cycles in its natural subterranean habitat. At the cellular level, these conditions are known to promote genomic instability, which underlies both cancer and aging. However, Spalax is a long-lived animal and is resistant to both spontaneous and induced cancers. To study this apparent paradox we utilized a computational procedure that allows detecting differences in transcript abundance between Spalax and the closely related above-ground Rattus norvegicus in individuals of different ages. Functional enrichment analysis showed that Spalax whole brain tissues maintain significantly higher normoxic mRNA levels of genes associated with DNA damage repair and DNA metabolism, yet keep significantly lower mRNA levels of genes involved in bioenergetics. Many of the genes that showed higher transcript abundance in Spalax are involved in DNA repair and metabolic pathways that, in other species, were shown to be downregulated under hypoxia, yet are required for overcoming replication- and oxidative-stress during the subsequent reoxygenation. We suggest that these differentially expressed genes may prevent the accumulation of DNA damage in mitotic and post-mitotic cells and defective resumption of replication in mitotic cells, thus maintaining genome integrity as an adaptation to acute hypoxia-reoxygenation cycles.

The double benefit of Spalax p53: surviving underground hypoxia while defying lung cancer cells in vitro via autophagy and caspase-dependent cell death.

The blind subterranean mole rat, Spalax ehrenbergi, is a model organism for hypoxia tolerance. This superspecies have adapted to severe environment by altering an array of hypoxia-mediated genes, among which an alteration in the p53 DNA binding domain (corresponding to R174K in humans) that hinders its transcriptional activity towards apoptotic genes. It is well accepted that apoptosis is not the only form of programmed cell death and that mechanisms that depend on autophagy are also involved. In the current work we have extended our research and investigated the possibility that Spalax p53 can activate autophagy. Using two complementary assays, we have established that over-expression of the Spalax p53 in p53-null cells (human lung cancer cells, H1299), potently induces autophagy. As Spalax is considered highly resistant to cancer, we further studied the relative contribution of autophagy on the outcome of H1299 cells, following transfection with Spalax p53. Results indicate that Spalax p53 acts as a tumor suppressor in lung cancer cells, inducing cell death that involves autophagy and caspases and inhibiting cell number, which is exclusively caspase-dependent. To conclude, the Spalax p53 protein was evolutionary adapted to survive severe underground hypoxia while retaining the ability to defy lung cancer.

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

Incipient sympatric speciation in blind mole rat, Spalax galili, in Israel, caused by sharp ecological divergence of abutting chalk-basalt 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 FST 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 ecological-genomic 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.

Non-image Forming Light Detection by Melanopsin, Rhodopsin, and Long-Middlewave (L/W) Cone Opsin in the Subterranean Blind Mole Rat, Spalax Ehrenbergi: Immunohistochemical Characterization, Distribution, and Connectivity.

The blind mole rat, Spalax ehrenbergi, can, despite severely degenerated eyes covered by fur, entrain to the daily light/dark cycle and adapt to seasonal changes due to an intact circadian timing system. The present study demonstrates that the Spalax retina contains a photoreceptor layer, an outer nuclear layer (ONL), an outer plexiform layer (OPL), an inner nuclear layer (INL), an inner plexiform layer (IPL), and a ganglion cell layer (GCL). By immunohistochemistry, the number of melanopsin (mRGCs) and non-melanopsin bearing retinal ganglion cells was analyzed in detail. Using the ganglion cell marker RNA-binding protein with multiple splicing (RBPMS) it was shown that the Spalax eye contains 890 ± 62 RGCs. Of these, 87% (752 ± 40) contain melanopsin (cell density 788 melanopsin RGCs/mm2). The remaining RGCs were shown to co-store Brn3a and calretinin. The melanopsin cells were located mainly in the GCL with projections forming two dendritic plexuses located in the inner part of the IPL and in the OPL. Few melanopsin dendrites were also found in the ONL. The Spalax retina is rich in rhodopsin and long/middle wave (L/M) cone opsin bearing photoreceptor cells. By using Ctbp2 as a marker for ribbon synapses, both rods and L/M cone ribbons containing pedicles in the OPL were found in close apposition with melanopsin dendrites in the outer plexus suggesting direct synaptic contact. A subset of cone bipolar cells and all photoreceptor cells contain recoverin while a subset of bipolar and amacrine cells contain calretinin. The calretinin expressing amacrine cells seemed to form synaptic contacts with rhodopsin containing photoreceptor cells in the OPL and contacts with melanopsin cell bodies and dendrites in the IPL. The study demonstrates the complex retinal circuitry used by the Spalax to detect light, and provides evidence for both melanopsin and non-melanopsin projecting pathways to the brain.

Controlling for Phylogenetic Relatedness and Evolutionary Rates Improves the Discovery of Associations Between Species' Phenotypic and Genomic Differences.

The growing number of sequenced genomes allows us now to address a key question in genetics and evolutionary biology: which genomic changes underlie particular phenotypic changes between species? Previously, we developed a computational framework called Forward Genomics that associates phenotypic to genomic differences by focusing on phenotypes that are independently lost in different lineages. However, our previous implementation had three main limitations. Here, we present two new Forward Genomics methods that overcome these limitations by (1) directly controlling for phylogenetic relatedness, (2) controlling for differences in evolutionary rates, and (3) computing a statistical significance. We demonstrate on large-scale simulated data and on real data that both new methods substantially improve the sensitivity to detect associations between phenotypic and genomic differences. We applied these new methods to detect genomic differences involved in the loss of vision in the blind mole rat and the cape golden mole, two independent subterranean mammals. Forward Genomics identified several genes that are enriched in functions related to eye development and the perception of light, as well as genes involved in the circadian rhythm. These new Forward Genomics methods represent a significant advance in our ability to discover the genomic basis underlying phenotypic differences between species. Source code: https://github.com/hillerlab/ForwardGenomics/

Sensitivity of primary fibroblasts in culture to atmospheric oxygen does not correlate with species lifespan.

Differences in the way human and mouse fibroblasts experience senescence in culture had long puzzled researchers. While senescence of human cells is mediated by telomere shortening, Parrinello et al. demonstrated that senescence of mouse cells is caused by extreme oxygen sensitivity. It was hypothesized that the striking difference in oxygen sensitivity between mouse and human cells explains their different rates of aging. To test if this hypothesis is broadly applicable, we cultured cells from 16 rodent species with diverse lifespans in 3% and 21% oxygen and compared their growth rates. Unexpectedly, fibroblasts derived from laboratory mouse strains were the only cells demonstrating extreme sensitivity to oxygen. Cells from hamster, muskrat, woodchuck, capybara, blind mole rat, paca, squirrel, beaver, naked mole rat and wild-caught mice were mildly sensitive to oxygen, while cells from rat, gerbil, deer mouse, chipmunk, guinea pig and chinchilla showed no difference in the growth rate between 3% and 21% oxygen. We conclude that, although the growth of primary fibroblasts is generally improved by maintaining cells in 3% oxygen, the extreme oxygen sensitivity is a peculiarity of laboratory mouse strains, possibly related to their very long telomeres, and fibroblast oxygen sensitivity does not directly correlate with species' lifespan.

The anti-tumor mechanisms in long-lived rodents

Rodents, including the nude mice with congenital aplasia of the thymus, cancer-resistant naked mole rat (Heterocephalus glaber) and blind mole rat (Spalax galili), are important model organisms that are widely used in biomedical research. The aging process is closely related to cancer incidence in mammals and the aging degree is positively correlated with the risk of cancer. Since rodents account for 40% of mammals, study of the unique antitumor mechanism in long-lived rodents is very important. Replicative senescence is anti-tumor mechanism that prevalently exist in rodents, however, unique anti-tumor mechanisms have been found in naked mole-rats and blind mole-rats. The cancer resistance of Spalax galili is mediated by cell-released IFN-β which activates p53 and Rb signaling pathway and the cells undergoes concerted cell death while that of Heterocephalus glaber is mediated by high molecular weight hyaluronan (HMW-HA) which causes contact inhibition. In addition, highly expressed pro-cell-death and anti-inflammation related genes are found in the genome of both naked mole-rats and blind mole-rats. In this review, we summarize the anti-tumor mechanisms in both Heterocephalus glaber and Spalax galili, which may provide information for related research.

Adaptive methylation regulation of p53 pathway in sympatric speciation of blind mole rats, Spalax

Epigenetic modifications play significant roles in adaptive evolution. The tumor suppressor p53, well known for controlling cell fate and maintaining genomic stability, is much less known as a master gene in environmental adaptation involving methylation modifications. The blind subterranean mole rat Spalax eherenbergi superspecies in Israel consists of four species that speciated peripatrically. Remarkably, the northern Galilee species Spalax galili (2n = 52) underwent adaptive ecological sympatric speciation, caused by the sharply divergent chalk and basalt ecologies. This was demonstrated by mitochondrial and nuclear genomic evidence. Here we show that the expression patterns of the p53 regulatory pathway diversified between the abutting sympatric populations of S. galili in sharply divergent chalk-basalt ecologies. We identified higher methylation on several sites of the p53 promoter in the population living in chalk soil (chalk population). Site mutagenesis showed that methylation on these sites linked to the transcriptional repression of p53 involving Cut-Like Homeobox 1 (Cux1), paired box 4 (Pax 4), Pax 6, and activator protein 1 (AP-1). Diverse expression levels of p53 between the incipiently sympatrically speciating chalk-basalt abutting populations of S. galili selectively affected cell-cycle arrest but not apoptosis. We hypothesize that methylation modification of p53 has adaptively shifted in supervising its target genes during sympatric speciation of S. galili to cope with the contrasting environmental stresses of the abutting divergent chalk-basalt ecologies.

Danger underground and in the open – predation on blind mole rats (Rodentia: Spalacinae) revisited

Abstract Being totally blind with no tail or pinnae, blind mole rats are the most specialised rodents for the subterranean lifestyle. However, they come to the surface occasionally due to unusual climatic events, for foraging, to collect hay for bedding material, for dispersal as subadults, due to intraspecific aggression, and in illness. The only previous review suggests that surface activity of and predation on blind mole rats is rare and that they are preyed on mainly at night by owls. Based on 57 scientific publications, 14 unpublished reports and several personal observations (from 15 countries), the present review reveals that altogether 26 species of bird and mammal prey on blind mole rats either regularly or occasionally. It is evidenced that not only the number of predators, but also the importance of blind mole rats in their diet has been seriously underestimated. The tight relationship between the colour of the soil and the colour of the pelage of blind mole rats suggests the importance of diurnal raptors via their selective impact. Predation by mammals happens relatively often, and mustelids hunt blind mole rats not only on the surface, but probably also inside their burrows. The labyrinth‐like structure of the burrows may play a vital role in confusing mammalian predators trying to hunt inside the burrows, and may increase the blind mole rat's chance of escape. With the proven importance of blind mole rats as a food resource for several threatened species of birds of prey, the survival, reproductive success, and population size of these species may partly depend on the density of the rodents. Although many species within the blind mole rat subfamily are themselves threatened to various extents, the role of blind mole rat populations in carnivore and raptor conservation should be considered and evaluated.

A novel metaheuristic for traveling salesman problem: blind mole-rat algorithm

Traveling Salesman Problem (TSP) is the problem of finding a minimum distance tour of cities beginning and ending at the same city and that each city are visited only once. As the number of cities increases, it is difficult to find an optimal solution by exact methods in a reasonable duration. Therefore, in recent five decades many heuristic solution methods inspired of nature and biology have been developed. In this paper, a new metaheuristic method inspired of the by-passing the obstacle strategy of blind mole rats living in their individual tunnel systems under the soil is designed for solving TSP. The method is called as Blind Mole-rat Algorithm. The proposed algorithm is tested on different size of symmetric TSP problems and the results are compared to the best known results. Initial test results are promising although proposed metaheuristic is not yet competitive enough among other algorithms in the literature. Keywords: Traveling salesman problem, Combinatorial optimization, Metaheuristic, Blind mole-Rat algorithm

Activity of free-living subterranean blind mole ratsSpalax galili(Rodentia: Spalacidae) in an area of supposed sympatric speciation

Subterranean rodents forage underground, which is energetically costly. Therefore, they can be expected to economize burrowing activity in response to food supply and soil characteristics. We analyzed the activity of radio-tracked blind mole rats, Spalax galili, on a locality sharply subdivided into harder but relatively food-rich, basaltic soil and softer, relatively food-poor rendzina. It was recently proposed that the mole rats in this locality are undergoing sympatric ecological speciation. We predicted that mole rats from basaltic soil would be less active than those from rendzina as a result of the reduced need for burrowing to reach food. By contrast to our predictions, mole rats from basaltic soil were more frequently located outside the nest and observed pushing soil above ground. We suggest that this is a result of territorial behaviour due to high population density. All mole rats exhibited a unimodal daily activity pattern likely related to temperature. Large males had large but gradually decreasing home-ranges, likely indicating the end of the mating season. We conclude that the ecological differences between the habitats cause behavioural differences in the mole rats, which indicates different selection pressures. The genetic divergence previously found between the populations might have arisen via density-dependent selection.