Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalax in Turkey

Karyotype (2fl) and allozymc diversity at 37 gene loci were determined in 69 subterranean mole rats in Turkey belonging to the two superspecies: the ancestor Spalax leucodon ( n = 55; 20 populations) and the descendant S. ehrenbergi ( n = 14; lour populations). We identified remarkable variation of diploid chromosome numbers in the S. leucodon superspecies: 2 n = 38. 40. 50, 54, 60 and 62; and in the S. ehrenbergi superspecies: 2 n = 52, 56 and 58. Genetic diversity indices were low on average in both S. leucodon and S. ehrenbergi superspecies: Allele diversity, A = 1.081 and 1.074; polymorphism, P-5%= 0.077 and 0.068; heterozygosity, H = 0.038 and 0.027; and gene diversity, H, = 0.038 and 0.034, respectively. H ranged from 0 in mesic or semimesic regions to 0.088 in arid Anatolia. We consider the populations with different diploid chromosome numbers, 2 n , as good biological species. Karyotypic diversity may mark extensive ecological speciation. Nei's genetic distances, D (average 0.174, range 0.002 0.422) and ecogeographical criteria suggest that almost each population may represent a different biological species, but critical future testing is necessary to support this claim. Karyotypes and allozymes are nonrandomly distributed across Turkey, displaying remarkable correlations with climatic and biolir factors. Both In and H are significantly correlated with aridity stress (2 n /rainfall, r , =–0.74; P < 0.001), and in our region also with climatic unpredictability. These results support the niche-width genetic variation hypothesis in space and time. Climatic selection in Turkey appears to be a major architect of karyotype and genetic (allozymc) diversity and divergence in mole rat evolution, in both speciation and adaptation.     

Taxonomic reassessment of Middle Eastern water frogs: Bioacoustic variation among populations considered as Rana ridibunda, R. bedriagae or R. levantina

Temporal characteristics of advertisement calls of water frogs of 10 localities in Turkey, Syria, Israel and Egypt were compared with those of Rana ridibunda in Kazakhstan, Armenia and Greece (Thrace) as reference populations. These study sites include the type localities of R. ridibunda , R. r. caralitana , R. esculenta var. bedriagae und R. levantina . The temperature-dependent as well as the temperature-independent call parameters clearly revealed two species. R. ridibunda is represented by the three reference populations and, in addition, a population in central Turkey. The other populations (in Turkey, Syria, Israel and Egypt) represent R. bedriagae . R. bedriagae is the oldest available name for water frogs of these regions and was given priority over R. r. caralitana and R. levantina .     

Seismic communication in the blind subterranean mole-rat: patterns of head thumping and of their detection in the Spalax ehrenbergi superspecies in Israel

Patterns of seismic communication and somatosensory responses were studied in four chromosomal species (2n= 52, 54, 58, 60) of blind subterranean mole-rats, belonging to the Spalax ehrenbergi superspecies in Israel. The patterns involved head thumping signals and surface-recorded cerebral potentials evoked by vibrational signals. The patterns correspond to the differences in territory size and population density which characterize the four species. It is suggested that this correspondence is related to the adaptive significance of the seismic communication.     

CYTOGENETICS OF HYBRIDS OF CARTHAMUS SPECIES (COMPOSITAE) WITH TEN PAIRS OF CHROMOSOMES

Plants thought to be typical of 7 species were chosen to represent the various taxa of Carthamus species with 10 pairs of chromosomes. These entities were crossed in all possible combinations and 20 of the possible 21 interspecific hybrids were obtained after 3 seasons of crosses. Analyses of the hybrids included studies of microsporocytes, pollen stainability, achene fertility, rudimentary ovaries, and other morphological characteristics. Pairing of chromosomes at metaphase I indicated no translocations were present in hybrids between C. tenuis from Israel, C. alexandrinus from Egypt, C. glaucus from northern Israel, and C. syriacus from Jordan. Members of this group are assigned the standard arrangement. Hybrids of C. glaucus from Iran, C. glaucus from Syria, and C. dentatus from Turkey always showed a translocation or chromosomal interchange when crossed with any member having the “standard” arrangement. The last 3 species are considered to have the “non-standard” chromosomal arrangement. The parental species used in this study can be regarded as a set of testers which will allow identification of chromosomal differentiation in additional Carthamus materials as they are collected.     

Penial differentiation in speciation of subterranean mole rats Spalax ehrenbergi in Israel

Geographic and ontogenetic variation was examined in the glans penes and bacula of 92 specimens representing four biological species with the karyotypes 2n=52, 54, 58 and 60 of the Spalax ehrenbergi superspecies in 13 populations from Israel and one disjunct population from northern Egypt. Five measured and three calculated penial characters were analysed and employed in multivariate statistics. Comparison was made between penial morphological characters and craniometric biochemical and chromosomal data. The baculum is strongly species-specific and its length bears no significant relationships with head and body length. The results of these analyses suggest that different bacular morphologies may provide a basis for species-specific prezygotic isolating mechanisms, thus, together with other factors, contributing to reproductive isolation and speciation.     

Chromosomal polymorphisms in subterranean mole rats: origins and evolutionary significance

Two distinct chromosomal polymorphisms, among others, characterize the short (p) and long (qh) arms of chromosome number 1 of the Spalax ehrenbergi complex in Israel. We have studied the geographic distributions of these two polymorphisms in 60 animals belonging to four chromosomal species (2 n = 52, 54, 58 and 60). These comprised 15 populations: 12 from continuously distributed populations, two from semi-isolates, and one isolate in the northern Negev Desert.
Our results indicate that: (i) the two polymorphisms are widespread not only within populations and species but most strikingly between different bone marrow cells within an individual; this may reflect a diversity generating mechanism; (ii) the two polymorphisms of p and qh, primarily of p, are correlated with climatic factors of water availability and temperature, as well as geographical distances; these correlations are significantly above those expected by chance, (iii) The semi-isolates and the isolate display high levels of polymorphism in both p and qh, but particularly in qh, despite the small size population effects.
We suggest that at least the polymorphism in p is involved in the adaptive radiation of mole rats into diverse climatic regimes. Furthermore, we speculate that the forces generating chromosomal polymorphisms relevant to speciation (i.e. Robertsonian mutations), coupled with the evolutionary forces operating in small peripherally isolated populations, may be appropriate for the origin of new chromosomal species through peripatric speciation.     

Mitochondrial DNA polymorphisms in subterranean mole-rats of the Spalax ehrenbergi superspecies in Israel, and its peripheral isolates

Patterns of mitochondrial DNA (mtDNA) variation were examined in 133 mole-rats constituting all four chromosomal species (2n = 52, 2n = 54, 2n = 58, and 2n = 60) of the Spalax ehrenbergi superspecies in Israel, as well as the peripheral isolates of 2n = 60. In the main range of the complex, a total of 28 mtDNA haplotypes were found in 64 mole-rats, with most haplotypes being unique to either a single chromosomal species or population. mtDNA divergence increased from low to high diploid number in a north-to-south direction in Israel. Overall levels of mtDNA diversity were unexpectedly the highest in the 2n = 60, the youngest species of the complex. The mtDNA haplotypes can be separated into two major groups, 2n = 52-54 and 2n = 58-60, and a phylogenetic analysis for each group revealed evidence of a few haplotypes not sorted by diploid number. The overall patterns of mtDNA divergence seen within and among the four chromosomal species are consistent with the parapatric mode of speciation as suggested from previous studies of allozyme and DNA hybridization. In a separate data set the patterns of mtDNA variation were examined across the main geographic range and across peripheral semi-isolates and isolates of the 2n = 60 chromosomal species. Fifteen haplotypes were found in 69 mole-rats. High levels of mtDNA diversity characterized the main range, semi-isolated, and even some desert isolated populations. The peripheral isolates contain much mtDNA diversity, including novel haplotypes.      

Additional records of the Ring-necked Parakeet,Psittacula krameri,from Egypt and the Middle East

Abstract

Additional new records and references from the literature are given for the Ring-nek-ked Parakeet, Psittacula krameri, in Egypt, Jordan, Israel and Syria. The species only succeeds in surviving in areas where there is little pressure from hunting, for example the city area of Cairo and several localities in Israel.     

Modelling the potential distribution of the Bridled Skink,Trachylepis vittata (Olivier, 1804), in the Middle East

The Bridled Skink, Trachylepis vittata, is widespread in the Middle East and eastern coastal Mediterranean areas and inhabits foothills throughout the arid regions of the Middle East. With the help of more than 146 distribution records from Iran, Turkey, Syria, Israel, Jordan, Cyprus, Egypt, Lebanon and Libya, we analysed the influence of climate on the distribution pattern. According to the Maximum Entropy model, the most influential factors that determined T. vittata distribution are: precipitation of coldest quarter, Normalised Difference Vegetation Index (NDVI) and precipitation in the warmest quarter. The model suggests that the western slopes of the Zagros Mountains in Iran and slopes in the southern regions of Anatolia around the Mediterranean Sea are suitable for this species. The species is associated with areas with intermediate NDVI (150-180) (a measure of primary productivity), high winter precipitation (>300?mm) and dry summer (<50mm). The association with rainy winter limits the presence of the species in lowlands. The Zagros Mountains may act as a biogeographic barrier that limits the species dispersal eastward, because of their scarce precipitation.     

Use of consensus sequences and genetic networks to identify members of the Bemisia tabaci cryptic species complex in Egypt and Syria

The sweet potato whitefly, Bemisia tabaci (Gennadius), is a cryptic species complex composed of at least 24 different morphologically indistinguishable species. The considerable differences in the pest status across the complex, and the ability of some to develop resistance to, insecticides make awareness of their identity critical in terms of developing effective control measures. Previously, phylogenetic reconstructions have been used to identify different B. tabaci, but this approach is no longer necessary because of the existence of mitochondrial cytochrome oxidase one consensus sequences for each of the known species. We therefore use these consensus sequences to determine the identities of the members of the complex in Syria and Egypt and then used genetic networks to reveal the pattern of their genetic relatedness to other haplotypes in the species to which they were assigned. The results showed the presence of three species in Syria, AsiaII 1, Middle East–Asia Minor 1 (this equates to the global invader known commonly as the B biotype) and Mediterranean (this equates to the global invader known commonly as the Q biotype). Egypt was shown to have two cryptic species, Middle East–Asia Minor 1 and Mediterranean. In Syria, Middle East–Asia Minor 1 was found around Damascus only (south‐west Syria), while Mediterranean was found throughout Aleppo (northern Syria) and Hama (north central Syria). AsiaII 1 was found around Hims (south central Syria) and Damascus (south‐western Syria). In Egypt, Mediterranean was found in Cairo and Ismailia (central Upper Egypt), while Middle East–Asia Minor 1 was found in the remaining all parts of Upper Egypt, Suez, North Sinai, Port Said, Dakahila, Behera and Alexandria which cover the main agricultural zone of Egypt. Genetic relatedness of Syrian and Egyptian populations with each other and with rest of world is also discussed.     

Variations in ribosomal DNA and mitochondrial DNA among chromosomal species of subterranean mole rats

Restriction site variations in nuclear ribosomal DNA (rDNA) spacers and mitochondrial DNA (mtDNA) were examined in several populations of mole rats with variable numbers of chromosomes, which represented the two superspecies Spalax leucodon (2n = 38, 54, or 62) and Spalax ehrenbergi (2n = 52, 54, 58, or 60). Sequence divergence of rDNA spacers between the members of the superspecies was approximately 8%, while the variation within each superspecies was 4% on average. The intrasuperspecies differentiation of rDNA spacers was generally associated with changes in the diploid number of chromosomes. However, substantial divergence (approximately 1.5%) was also detected among populations with the same diploid number of chromosomes. The sequence divergence of mtDNA among haplotypes of S. ehrenbergi was 10% or higher and among haplotypes of S. leucodon it was approximately 12%. By contrast, the range of sequence divergence between superspecies was 7.4%-12%. The large divergence of mtDNAs within each superspecies of mole rats may be explained by the preservation of ancient mtDNA polymorphisms.      

Taxonomic reassessment of Middle Eastern water frogs: Morphological variation among populations considered as Rana ridibunda, R. bedriagae or R. levantina

Eight morphometric features of water frogs of 14 localities in Turkey, Syria, Jordan and Israel were compared with those of Rana ridibunda in Kazakhstan, Armenia and Greece (Thrace). These study sites include the type localities of R. ridibunda , R. r. caralitana , R. esculenta var. bedriagae and R. levantina . Multivariate comparisons (principal-component analysis, discriminant analysis) based on the log₁₀-transformed variables demonstrate that the data set includes only two taxa that differ significantly in size and shape. By applying a morphospecies criterion, R. ridibunda is represented exclusively by the three reference populations, whereas all other populations (in Turkey, Syria, Jordan and Israel) represent the same species , R. bedriagae .     

Genetic structure of Mediterranean populations of the sandfly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis

Phlebotomus papatasi (Scopoli) (Diptera: Psychodidae) is the main vector of Leishmania major Yakimoff & Schokhor; which is the cause of self-limiting cutaneous leishmaniasis in the Old World. This sandfly is found in houses, animal shelters, caves and rodent burrows. It has a large geographical range, which includes the Middle East and the Mediterranean regions. A population analysis of colony and field specimens of P. papatasi was conducted on 25 populations originating from 10 countries. The distribution of haplotypes of the maternally inherited mitochondrial cytochrome b gene were analysed to assess the population differentiation of P. papatasi. Alignment of a 442-basepair region at the 3' end of the gene identified 21 haplotypes and 33 segregating sites from 131 sandflies. The pattern of sequence variations did not support the existence of a species complex. The median-joining network method was used to describe both the origin of the haplotypes and the population structure; haplotypes tended to cluster by geographical location, suggesting some level of genetic differentiation between populations. Our findings indicate the presence of significant population differentiation for populations derived from Syria, Turkey, Palestine, Israel, Jordan and Egypt. Knowledge of population differentiation among P. papatasi populations is important for understanding patterns of dispersal in this species and for planning appropriate control measures.     

Mhc Class II DNA Polymorphisms within and between Chromosomal Species of the Spalax Ehrenbergi Superspecies in Israel

Restriction fragment length polymorphisms (RFLPs) of two major histocompatibility class II genes (P alpha 1 and Q beta) were studied in 13 populations of four chromosomal species (2n = 52, 54, 58 and 60) of the mole rat, Spalax ehrenbergi superspecies in Israel. A substantial frequency of allelic fragments was found in both genes for all populations, including a desert isolate. In the P alpha 1 gene, one allelic fragment is a result of a deletion mutation which is diagnostic of the 2n = 52 chromosomal species. All other ten allelic variants are the result of point mutations. All mutations are located in a short region flanking the 3' end of the gene. Based on Mhc polymorphisms we confirm earlier evidence that gene flow does not occur between the older chromosomal species (2n = 52, 54, 58), and that reproductive isolation decreases, progressively from the oldest to the youngest species (2n = 60).     

Burrow patterns of the mole rat Spalax ehrenbergi in two soil types (terra-rossa and rendzina) in Mount Carmel, Israel

Complete burrow systems of the mole rat Spalax ehrenbergi (Rodentia; Spalacidae), from two sites on Mount Carmel in Israel, with different soil types (terra-rossa and rendzina), were excavated and described here for the first time.
A comparison was made of burrow structure patterns in the two soils and of the sexes, with special attention to the features of the feeding tunnels.
The pattern in the rendzina revealed longer burrows with a longer main tunnel and fewer branches per metre of the main tunnel, while the pattern in the terra-rossa revealed shorter burrows with a shorter main tunnel and a relatively higher number of branches. These differences can primarily be related to the different levels of food availability, which is higher in the terra-rossa. It is suggested that each of the patterns reflects the mole rat's ability to optimize foraging efficiency in accordance with its given food availability.
The average total length of the males' burrows was much greater than those of the females' burrows in the rendzina soil. It appears that food requirements determine different burrow features of the sexes rather than reproduction requirements.
Other tunnel features (e.g. structural complexity, depth and width, segment length and spatial arrangement) and the factors which may affect them, as well as burrow structure of young mole rats and evidence of the underground dispersion of young mole rats, were presented and discussed.
Many similarities were found in a comparison of S. ehrenbergi burrow features with those of other solitary subterranean rodents.     

Late Pleistocene and Holocene equid remains from Israel

Equid remains–mostly isolated teeth–from archaeological sites in Israel are described. Particular attention is paid to dental enamel fold morphology and criteria are established tor separating several Old World Quaternary equid species. Eauus hydruntinus , which is here considered a zebra rather than an ass, was present until 12,000 bp in northern Israel, while at the same time E-asinus/hemionus inhabited the arid regions in the south. Inirequent remains of E. caballus are also described. By 4000 years ago ass, probably the domestic form, was present in northern Israel.     

New species of mole crickets of the Gryllotalpa gryllotalpa group (Orthoptera: Gryllotalpidae) from Israel, based on morphology, song recordings, chromosomes and cuticular hydrocarbons, with comments on the distribution of the group in Europe and the Mediterranean region

Two sibling species of mole crickets of the Gryllotalpa gryllotalpa group inhabit Israel. Both are described as new species based on differences in their morphology, acoustic behaviour, chromosome number, cuticular hydrocarbon pattern and habitats. The species with males having 2n = 23 chromosomes, described in the past as the 'Dead Sea race', is designated as G. marismortui sp.n. It is an endangered species. In morphology and chromosome number it is similar to G. cossyrensis Bacetti & Capra from Italy, but differs in the composition of cuticular hydrocarbons. Gryllotalpa marismortui occurs in a limited geographical area along the shore of the Dead Sea. Another species, with 2n = 19 chromosomes, is described as G. tali sp.n. and is found throughout Israel. The calling songs of the males of the new species differ markedly. Females of the respective chromosomal numbers discriminate in favour of the homospecific call. Their habitats are strikingly different: G. marismortui lives in hypersaline soil along the Dead Sea shore (total chloride 187.25 meq %), G. tali inhabits freshwater soil (9.31 meq %). The distribution of the twelve known sibling species and one chromosomal race (not yet described) of the G. gryllotalpa group from Europe and the eastern Mediterranean is summarized. The zoogeography and phylogeny of the group are discussed.     

Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic-hypercapnic stresses

The composition of oxygen (O2), carbon dioxide (CO2), and soil humidity in the underground burrows from three species of the Israeli subterranean mole rat Spalax ehrenbergi superspecies were studied in their natural habitat. Two geographically close populations of each species from contrasting soil types were probed. Maximal CO2 levels (6.1%) and minimal O2 levels (7.2%) were recorded in northern Israel in the breeding mounds of S. carmeli in a flooded, poor drained field of heavy clay soil with very high volumetric water content. The patterns of gas fluctuations during the measurement period among the different Spalax species studied were similar. The more significant differentiation in gas levels was not among species, but between neighboring populations inhabiting heavy soils or light soils: O2 was lower and CO2 was higher in the heavy soils (clay and basaltic) compared to the relatively light soils (terra rossa and rendzina). The extreme values of gas concentration, which occurred during the rainy season, seemed to fluctuate with partial flooding of the tunnels, animal digging activity, and over-crowded breeding mounds inhabited by a nursing female and her offspring. The gas composition and soil water content in neighboring sites with different soil types indicated large differences in the levels of hypoxic-hypercapnic stress in different populations of the same species. A growing number of genes associated with hypoxic stress have been shown to exhibit structural and functional differences between the subterranean Spalax and the above-ground rat (Rattus norvegicus), probably reflecting the molecular adaptations that Spalax went through during 40 million years of evolution to survive efficiently in the severe fluctuations in gas composition in the underground habitat.     

The effect of protein and salt loading on urinary concentrating ability in four chromosomal species of Spalax ehrenbergi

Urinary concentrating ability was tested under protein and salt load in the four chromosomal species of subterranean mole-rats ( Spalax ehrenbergi superspecies) found in Israel. Protein stress induced by a diet of soyabeans supplemented by agar gel, demonstrated a significant increase in urinary osmolarity (UO). In the species living in the driest and warmest region (2n = 60). UO (1423·101 mOsmol/kg) was significantly (P<0·05) higher than in the other three species (2n = 52. 1172·31 mOsmol/kg; 2n = 54, 1160·116 mOsmol kg; and 2n = 58, 1216·145 mOsmol/kg). Upon salt loading this diet with 0·3 mol NaCl, UO increased significantly. However, when the salt load was increased to 0·45 mol NaCl, UO decreased significantly in all but one species (2n = 60) which maintained UO at 1522·65 mOsmol/kg. A decline in UO was attributed to diuresis resulting from a significant increase in urine and sodium excretion. The kidney, of only the xeric ranging species (2n = 60), demonstrated the ability to produce a hyperosmotic urine, in spite of the high salt load. These results might explain the restricted distribution of S. ehrenbergi: the only species (2n = 60) found in an environment rich in succulents and halophyte plants (steppe). This species appears to push speciation and adaptive radiation to the southern limit of its superspecies.     

Brain size diversity in adaptation and speciation of subterranean mole rats

We have tested brain size diversity and encephalization in the actively speciating subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. Our sample involved 171 individuals comprising 12 populations and 4 chromosomal species (2n = 52, 54, 58 and 60) distributed parapatrically from the northern Mediterranean region southward (2n = 52, 54→+58→60) into increasingly more arid and unpredictable climatic regimes, approaching the Negev Desert. Our results indicate that relative brain size and encephalization are highest in 2n = 60 as compared with 2n = 52, 54 and 58. We hypothesize that this pattern is adaptive and molded by natural selection. Brain evolution and higher encephalization in the S. ehrenbergi complex appears to be associated with increasing ecological stresses of aridity and climatic unpredictability.