Species Of Spermophilus Research Articles

Traditional multilocus phylogeny fails to fully resolve Palearctic ground squirrels (Spermophilus) relationships but reveals a new species endemic to West Siberia

Previous efforts to reconstruct evolutionary history of Palearctic ground squirrels within the genus Spermophilus have primarily relied on a single mitochondrial marker for phylogenetic data. In this study, we present the first phylogeny with comprehensive taxon sampling of Spermophilus via a conventional multilocus approach utilizing five mitochondrial and five nuclear markers. Through application of the multispecies coalescent model, we constructed a species tree revealing four distinct clades that diverged during the Late Miocene. These clades are 1) S. alaschanicus and S. dauricus from East Asia; 2) S. musicus and S. pygmaeus from East Europe and northwestern Central Asia; 3) the subgenus Colobotis found across Central Asia and its adjacent regions and encompassing S. brevicauda, S. erythrogenys, S. fulvus, S. major, S. pallidicauda, S. ralli, S. relictus, S. selevini, and S. vorontsovi sp. nov.; and 4) a Central/Eastern Europe and Asia Minor clade comprising S. citellus, S. taurensis, S. xanthoprymnus, S. suslicus, and S. odessanus. The latter clade lacked strong support owing to uncertainty of taxonomic placement of S. odessanus and S. suslicus. Resolving relationships within the subgenus Colobotis, which radiated rapidly, remains challenging likely because of incomplete lineage sorting and introgressive hybridization. Most of modern Spermophilus species diversified during the Early–Middle Pleistocene (2.2–1.0 million years ago). We propose a revised taxonomic classification for the genus Spermophilus by recognizing 18 species including a newly identified one (S. vorontsovi sp. nov.), which is found only in a limited area in the southeast of West Siberia. Employing genome-wide single-nucleotide polymorphism genotyping, we substantiated the role of the Ob River as a major barrier ensuring robust isolation of this taxon from S. erythrogenys. Despite its inherent limitations, the traditional multilocus approach remains a valuable tool for resolving relationships and can provide important insights into otherwise poorly understood groups. It is imperative to recognize that additional efforts are needed to definitively determine phylogenetic relationships between certain species of Palearctic ground squirrels.

Surrounded by Kindred: Spermophilus major Hybridization with Other Spermophilus Species in Space and Time.

Among the numerous described cases of hybridization in mammals, the most intriguing are (a) cases of introgressive hybridization deeply affecting the evolutionary history of species, and (b) models involving not a pair of species but a multi-species complex. Therefore, the hybridization history of the russet ground squirrel Spermophilus major, whose range has repeatedly changed due to climatic fluctuations and now borders the ranges of four related species, is of great interest. The main aims of this study were to determine the direction and intensity of gene introgression, the spatial depth of the infiltration of extraneous genes into the S. major range, and to refine the hypothesis of the hybridogenic replacement of mitochondrial genomes in the studied group. Using phylogenetic analysis of the variability of mitochondrial (CR, cytb) and nuclear (SmcY, BGN, PRKCI, c-myc, i6p53) markers, we determined the contribution of neighboring species to the S. major genome. We showed that 36% of S. major individuals had extraneous alleles. All peripheral species that were in contact with S. major contributed towards its genetic variability. We also proposed a hypothesis for the sequence and localization of serial hybridization events. Our assessment of the S. major genome implications of introgression highlights the importance of implementing conservation measures to protect this species.

Lithologic features of near-surface layers of the Quaternary cover as a key to understanding of environmental constraints for the Quaternary ground squirrel species

ABSTRACT Here, we propose the modern soil map as a source for creating spatial context for agent-based modelling of the historical expansion and dispersal of ground squirrel species. On the basis of this soil map, we produced a lithologic map of the near-surface layers of the Quaternary cover. Units of this new lithologic map (i.e. certain kinds of substrate) were assessed in context of preferability by certain ground squirrel species. Then, these (basic) preference rates were modified for the case of valley slopes (positive impact of valley slopes) and for the case of loess-and-soil accumulation (also positive impact). The hypothesis of the positive impact of loess and soil accumulation is supported by following facts: range shrinking of Spermophilus species in the Holocene; stability of the range boundary between Spermophilus pygmaeus and Spermophilus suslicus in the Middle and Late Pleistocene and the ability of the Pleistocene ecosystems to support high animal biomass even during cold epochs.

Quaternary evolution of the river Danube in the central Pannonian Basin and its possible role as an ecological barrier to the dispersal of ground squirrels

ABSTRACT Large rivers can act as important ecological barriers for small mammals, but their exact role is debated. Here we examine the effect of the river Danube on populations of the European ground squirrel, an important representative of steppe communities, by studying the Quaternary history both of ground squirrels and of the Danube in the Pannonian Basin, in Hungary. The Danube experienced considerable channel changes during the Quaternary, with >100 km westward shift of its middle reach, interrupted by temporary eastward movements. Besides autogenic river processes, tectonically induced avulsions have played a role in re-routing channels. Three of the four Spermophilus species certainly extended their ranges on both sides of the Danube, referring to repeated river crossings during the Quaternary. Hydrological events, most importantly rapid river course changes (avulsions) but also meander cut-offs are viable mechanisms to enable ground squirrel populations to cross large rivers. On longer timescales, oscillating river course changes can maintain gene exchange across the river.

‘Good fences make good neighbours’: Concepts and records of range dynamics in ground squirrels and geographical barriers in the Pleistocene of the Circum-Black Sea area

Ground squirrels were an important member of the Pleistocene steppe-tundra mammal community. They evolved ecological specialisations and exhibit behaviours that make them particularly informative subjects to study palaeoenvironmental constraints affecting species distribution and speciation. Interspecific competition and isolating geographical barriers are considered as the principal factors that define species range boundaries.The present paper provides a first comprehensive compilation of the living and extinct Spermophilus species in Europe. These data suggest ‘patchwork quilt’ model for the expansion and spatial distribution of ground squirrel species. Here we consider mainly small-sized Spermophilus species because large-sized (e.g., S. superciliosus) ground squirrels consist another ‘patchwork quilt’, which overlap the first one. This overlapping of the species ranges is possible because of the size difference that lowers interspecific competition (Hutchinson's rule).We consider two main types of range boundaries. One type includes roughly ‘sub-parallel’ boundaries that oscillate in concert with climatic and vegetational changes (a case of climatically controlled competitive exclusion). The other type consists of roughly ‘sub-meridional’ boundaries corresponding to geographical barriers (e.g., water barriers, mountain ridges); these boundaries are rather stable. Examples of ‘sub-parallel range modifications include: oscillations of boundaries between S. pygmaeus and S. suslicus; the immigration of S. citellus into the Pre-Carpathian area; the branching of S. suslicus from S. pygmaeus; the regional appearance of the Late Pleistocene species S. severskensis and S. citelloides. Examples of ‘sub-meridional events’ are: the crossing of the Danube by S. citellus; the appearance of an isolated population of S. pygmaeus on right bank of the Dnieper during the Late Pleistocene to Middle Holocene; a crossing of the Dnieper river by S. pygmaeus, which resulted in the appearance of S. odessanus; the intrusion of eastern populations of S. pygmaeus into the Trans-Volga areas.

Phylogeny of genus Spermophilus and position of Alashan ground squirrel (Spermophilus alashanicus, Buchner, 1888) on phylogenetic tree of Paleartic short-tailed ground squirrels

Phylogenetic relationships within a group of Paleartic short tailed ground squirrels (Spermophilus), recently defined as genus, are not sufficiently clear and need a critical revision. Interspecies hybridization, found in Eurasian Spermophilus, can affect the results of reconstruction of molecular phylogeny. Alashan ground squirrel position on the phylogenetic tree needs clarification. We analyzed eight nucleotide sequences of cytb gene of S. alashanicus and 127 sequences of other Spermophilus species form GenBank. S.alashanicus and S. dauricus close phylogenetic relationship, and their affinity to ancestral forms of the group are revealed. Monophyly of Colobotis subgenus was confirmed. Paraphyly of eastern and western forms of S. relictus was shown.

Reconstruction of karyotype evolution in core Glires. I. The genome homology revealed by comparative chromosome painting

Glires represent a eutherian clade consisting of rodents and lagomorphs (hares, rabbits, and pikas). Chromosome evolution of Glires is known to have variable rates in different groups: from slowly evolving lagomorphs and squirrels to extremely rapidly evolving muroids. Previous interordinal homology maps between slowly evolving Glires were based on comparison with humans. Here, we used sets of chromosome-specific probes from Tamias sibiricus (Sciuridae), Castor fiber (Castoridae) and humans to study karyotypes of six ground squirrels (genera Marmota and Spermophilus) and one tree squirrel (genus Sciurus), mountain hare (genus Lepus), and rabbit (genus Oryctolagus). These data supplemented with GTG banding comparisons allowed us to build comparative chromosome maps. Our data showed the absence of previously found squirrel associations HSA 1/8 and 2/17 in the Eurasian ground squirrels--sousliks and woodchucks, and disruptions of squirrel HSA 10/13 and HSA 8/4/8/12/22 syntenies in the four Spermophilus species studied here. We found that the karyotypes of Sciuridae and Leporidae are highly conserved and close to the Rodentia ancestral karyotype, while Castoridae chromosomes underwent many more changes. We suggest that Lagomorpha and Sciuridae (in contrast to all other rodent families) should be considered as core Glires lineages, characterized by cytogenetically conserved karyotypes which contain chromosomal elements inherent to karyotype of common Glires ancestor. Our data allowed us to further refine the putative ancestral karyotypes of Rodentia. We also describe here the putative ancestral karyotypes of Glires and lagomorphs.

Is the Torpor-Arousal Cycle of Hibernation Controlled by a Non-Temperature-Compensated Circadian Clock?

During the hibernation season, mammalian hibernators alternate between prolonged bouts of torpor with a reduced body temperature (Tb) and short arousals with a return to euthermy. Evidence is presented here to show that this metabolic-and also physiological and neuroanatomical-rhythm is controlled by a clock, the torpor-arousal (TA) clock. The temperature dependence of torpor bout duration in 3 species of Spermophilus (published data) may be described by assuming that the TA clock is a circadian clock (probably not the suprachiasmatic clock) that has lost its temperature compensation. This loss might result either from a permanent deletion, or more likely from a seasonal epigenetic control at the level of the clock gene machinery. This hypothesis was verified over the full Tb range on published data from 5 other species (a monotreme, a marsupial, and 3 placental mammals). In a hibernation season, instantaneous subjective time of the putative TA clock was summated over each torpor bout. For each animal, torpor bout length (TBL) was accurately predicted as a constant fraction of a subjective day, for actual durations in astronomical time varying between 4 and 13 to 20 days. The resulting temperature dependence of the interval between arousals predicts that energy expenditure over the hibernation season will be minimal when Tb is as low as possible without eliciting cold thermogenesis.

Occurrence of scarab beetles inside rodent burrows in some parts of Iran (Coleoptera: Scarabaeidae)

The scarab beetles Ateuchetus armeniacus (Ménétries, 1832) and Gymnopleurus flagellatus (Fabricius, 1787) (Coleoptera, Scarabaeidae) are recorded for the first time inside burrows of two Spermophilus species (Mammalia). The observations concern nests of Spermophilus fulvus (Lichtenstein, 1823) in eastern, northwestern and western Iran, and Spermophilus xanthoprymnus (Bennet, 1835) in northwestern Iran. Neither of these beetles was known to be associated, not even occasionally, with burrows of small mammals.

Taxonomic status of the genus Spermophilus (Mammalia: Rodentia) in Turkey and Iran with description of a new species

We report a new species of Spermophilus ( Rodentia: Sciuridae), here designated as S. torosensis sp. nov., distributed in the Taurus Mountains in southern Anatolia, Turkey. A total of 161 specimens of the genus Spermophilus from Turkey and Iran were analyzed for their morphological, morphometric, and karyological characteristics. Uni- and multi-variate statistical analyses of morphologic data for 95 adult specimens yielded 4 distinct groups. Taxonomic evaluations classified the specimens into 4 species Spermophilus citellus, S. xanthopymnus, S. fulvus and S. torosensis sp. nov. Morphometrics, coat coloration, a brush-shaped tail, and a NFa value of 72 are diagnostic characters that distinguish S. torosensis sp. nov. from the other species. In Turkey, S. torosensis sp. nov. was found in 6 locations. The karyotype of S. fulvus also is described for the first time as 2n= 36, NFa= 70 and NFa= 66; new karyotypic data is reported for S. xanthoprymnus from Iran and Turkey.

Sex and Age Differences in Mass, Morphology, and Annual Cycle in European Ground Squirrels, Spermophilus citellus

We collected 6 years of data (1990-1995) on survival, hibernation, body-mass changes, and morphological parameters for a suburban population of European ground squirrels (Spermophilus citellus) using censusing and capture-recapture techniques. We attempted to determine differences in sex and age in these parameters. In the focal population, sex ratios of adults and yearlings were female-biased, but the sex ratio of juveniles was balanced. Overwinter mortality was low, but losses during the active season were high in all sex and age groups. Male and female juveniles disappeared from their natal area in roughly equal proportions. Among older individuals, more males disappeared than females. Hibernation patterns were similar to other Spermophilus species, except that females began hibernation before males. Therefore, females had significantly longer hibernation periods and higher proportional overwinter losses of mass than males. All adult (greater than or equal to 2 years) but only a few yearling males were reproductively active. Yearling males emerged from hibernation with a lower mass than adults but were indistinguishable from them before subsequent immergence. Adult and yearling females reproduced and lost mass during late lactation, a pattern more pronounced in older than yearling females. Juvenile males were heavier than juvenile females before hibernation, although no difference was found at weaning. Skull size increased in the first two active seasons but did not change thereafter. Differences in sex and age resembled those of most hibernating,ground squirrels in many aspects but also showed some unusual patterns that probably have evolved due to specific environmental constraints in this species.

Sexual differences in interyear survival and life-span of Richardson's ground squirrels

Although equal numbers of males and females were weaned in a population of Richardson's ground squirrels studied in southern Alberta, interyear survival was lower for males than for females in each year of life. Consequently, the sex ratio was biased toward females in both the yearling and older adult cohorts (overall ≤ 23 males per 100 females), and maximum life-span of males was 4 years, whereas that of females was 6 years. Compared with several other species of Spermophilus, Richardson's ground squirrels have a larger litter size at birth and a shorter life-span.

Immunological Systematics of Prairie Dogs

Relationships within the genus Cynomys were investigated using immunoelectrophoretic characters. A method is presented for coding these characters, by which numerical phylogenies can be constructed. No intraspecific differences were observed within Cynomys . Within the white-tailed group, C. leucurus and C. parvidens are antigenically similar, whereas C. gunnisoni appears more distantly related, although retaining many of the white-tailed characteristics. In the black-tailed group, C. ludovicianus and C. mexicanus appeared antigenically similar, but differentiated in two characters. The white-tailed and black-tailed groups are distinct lineages. The relationships of these two lineages to the Spermophilus species examined is unresolved.

Temporal overlap of female kin in Columbian ground squirrels (Spermophilus columbianus)

Columbian ground squirrels (Spermophilus columbianus) were live-trapped from 5 to 7 years at three sites in southwestern Alberta, Canada. The two most common adult matrilineal relatives for 2-year-old females were the mother and a 1 year older non-littermate sister. Co-occurrence of female kin depended firstly on size and sexual composition of litters and secondly on age-specific survival and recruitment rates. Adult matrilineal kin frequently coexisted among breeding females of this species, leading us to predict a social system strorgly influenced by nepotism. However, the life history traits of S. columbianus suggest an adult female kin cluster unlike that found for other species of Spermophilus in which littermate sisters are common. If availability of adult female kin influences kin-differential behaviour, then female S. columbianus should favour mothers, daughters and non-ittermate sisters.

Postnatal Growth and Development of Captive Franklin's Ground Squirrels (Spermophilus franklinii)

Growth and development of Franklin's ground squirrels (Spermophilus franklinii) were determined from 87 young raised by wild-caught females in the laboratory. Developmental stages appeared in the same sequence, but at a mean earlier age than in any other species of Spermophilus except S. undulatus. Lower incisors erupted on day 7, eyes and ears opened on day 20, and weaning occurred by day 28. Weight reached 25% of adult weight by day 34, 50% by day 44, 75% by day 54, and adult weight was reached by day 65. The instantaneous growth rate (IGR) was greatest in the 1st 10 days, with a maximum of 12.4% per day at day 3, decreasing to 1.2% by day 50. Hind foot length reached 75% of adult size by day 30, whereas total and tail lengths were less than 60% at the same age. Individual weight was negatively correlated with litter size, and there were indications of lower survival to weaning in numerically larger litters. Laboratory growth measurements cannot be directly extrapolated to field populations, since weaned laboratory young gained weight significantly more rapidly than field young. Data from similar studies on other hibernating sciurids suggest that birth dates and IGRs are related, and indicate a biological response to differing climates.

Ectoparasites from three species of Spermophilus (Rodentia: Sciuridae) in Alberta

Total populations of ectoparasites were obtained from 9 Spermophilus columbianus, 3 S. franklinti, and 63 S. richardsonii ground squirrels. These ectoparasites included 2 species of lice, 7 species of fleas, 1 species of tick, and 11 species of mites (only 2 of which are ground squirrel parasites). Comparisons were made for S. richardsonii to determine if ground squirrel age or sex had any effect upon burdens of lice and fleas. A list of free-living mites collected from these three species of Spermophilus is given together with a discussion of their association with ground squirrels.

Heterogeneity of Muscle Fibers in Some Burrowing Mammals

Proportional differences in type of fibers within homologous muscles of different burrowing mammals may be a paramount factor determining variation in strength, especially in the relatively unspecialized diggers. The proportions of types of fibers in seven pectoral muscles from two individuals of each of three species of Spermophilus , one species of Scapanus , and one species of Eutamias are demonstrated by comparing variations in glycogen content and differences in diameter. Results indicate the number and kinds of motor units present and thus something about potential gradations in tension. In all species of Spermophilus , muscles showed marked heterogeneity with red fibers predominating. Juveniles of S. beecheyi had a greater proportion of red fibers in most muscles compared to adults, which had a greater proportion of white fibers. This is attributed to ontogenetic change from relatively slow contracting muscles at birth to faster muscles in the adult. Muscles of Eutamias amoenus were primarily red-fibered, which is associated with the high metabolic rate for this species. Muscle fibers of Scapanus latimanus contained high amounts of glycogen but resembled the red fibers of ground squirrels in diameter. Differences in strength between the species of Spermophilus are probably not due to heterogeneity because of the similarity in this factor between muscles. Differences in strength of Scapanus latimanus and Eutamias amoenus when compared to the three species of Spermophilus may be due partly to differences in heterogeneity of muscles. When the proportions of fiber type within a muscle approach equality this implies a greater potential number of motor units that can be recruited. I believe that the heterogeneous muscles of ground squirrels allow the development of relatively great forces, whereas moles develop large forces because of more muscle per body weight and greater mechanical advantage.

Serum protein electrophoresis in the taxonomy of some species of the ground squirrel subgenus spermophilus

1. 1. Serum protein patterns of Sperhophilus undulatus, Spermophilus columbianus and Spermophilus beldingi were analyzed by two-dimensional starch-gel electrophoresis. 2. 2. The patterns, although generally similar, exhibited variation in nine fractions or groups of fractions and these fractions had taxonomic significance at the level of population, subspecies or species. Intraspecific variability of two unidentified protein fraction was observed in S. undulatus kennicotti and S. beldingi and a third protein polymorphism involving transferrin was also observed in S. undulatus kennicotti. Intraspecific divergence between Artic and sub-Arctic subspecies of S. undulatus was found and proteins from the latter show a closer resemblance to S. columbianus. 3. 3. The protein characters support present taxonomic concepts of the species of Spermophilus that indicate a close relationship between all three species and a closer relationship between S. undulatus and S. columbianus. 4. 4. Protein characters, as observed in the genus Spermophilus, appear to offer great promise as a method for systematic investigation at intraspecific levels where gross morphologic characters are least definitive.

Chromosome studies in certain subgenera of Spermophilus.

SummaryMitotic chromosomes of 3 species of Spermophilus have been analyzed. The diploid chromosome number was 30 in S. beldingi beldingi, 34 in S. tridecemlineatus tridecemlineatus and 36 in S. tereticaudus neglectus. Karyograms of 5. tridecemlineatus and S. beldingi were compared with karyograms of S. mexicanus and S. richardsonii. Differences in karyotype were demonstrated and discussed in relation to the classification of the genus Spermophilus. Karyograms of S. tereticaudus were different from other species of Spermophilus which supported its subgeneric status. The minute metacentric Y chromosome observed in S. beldingi differs from the larger acrocentric Y of other species of Spermophilus. The utilization of chromosome analysis in comparative taxonomy of the genus Spermophilus was demonstrated.The author wishes to thank Dr. F. del Greco for help and advice in preparing the manuscript.

Scientific Serials

Verhandlungen der k. k. zoologisch-botanischen Gesellschaft in Wicn, vol. xxv. The following papers are published in this volume: On some new species of Mycetophilidæ from the neighbourhood of Sandez (Galizia), by Dr. A. Grzegorzek.—On the structure of the muscular cells and on the general structure of Mnesira parasites, Krohn, by Prof. C. Claus.—On some new and some insufficiently known species of Cecidomyidæ of the Vienna district, by Dr. Franz Löw.—On the relations of the African and Indo-Malayan bird-fauna, with some general remarks on the geographical distribution of mammals, by A, von Pelzeln. —On Hungarian fungi (third treatise: fungi hypogæi), by Prof. A. Haszlinsky.—Description of new and insufficiently known Phryganidæ and Oestridæ, by Dr. Fr. Brauer.—Mycological notes, by S. Schulzervon Müggenburg.—Hemiplera Heteroptera Ausirmca, MM. Maji.—Augusti, 1870, a J. A. Palmén collecta, by O. M. Reuter.—On some new Lepidoptera of the South American fauna, by Dr. O. Staudinger.—Second note on the Arachnida-order of Territelariæ Thorrell (Mygalidæ Autor.), by Dr. Anton Ausserer. This is one of the most elaborate papers in the volume. On North-American moths, specially microlepidoptera, by Prof. P. C. Zeller; this is equally elaborate.— Notes on Adriatic echinoidæ, by Dr. E. von Maienzeller.—On the vegetation-formations of the Taurian peninsula and its climatic conditions, by Dr. A. Rehmann.—Researches on the Diptera-fauna of Austria, by Josef Palm.—On the ornithological fauna of Moravia, by F. von Dalberg.—On the occurrence of Salix bakylonica, L,., androgyna et masculina in Austria, by J. E. Hibsch.—Lichenological excursions in the Tyrol, by F. Arnld. —On some species of Salix new in the “Wechsel” district (Lower Austria), by E. Woloszczak. — Researches on land-Isopoda, byC. von Vogl.—On some species of Spermophilus, by Ernst Schauer.—On the fungi-flora of Bohemia, by F. von Thümen. —On the occurrence of short-eared Arvicolæ near Vienna, by Prof. L. H. Jeitteles.—On thermal constants and the power of accommodation in the vegetable kingdom, by Prof. H. Hoffmann.—Remarks on some ferns from the island of Celebes, by M. Kuhn.—Botanical excursions in Italy, by Dr. C. von Marchesetti.—Researches on some parasites infecting the hop plant, producing mildew and “kupferbrand”(copperburn), by Wilh. Voss.—Second paper, containing additional remarks on the Cecidomyidæ of the Vienna district, by Dr. Franz Löw.—Researches on Æolidiadæ, by Dr. R. Bergh.—New researches on Phyllidiadæ, by ihe same.—European Encyrtidæ, considered biologically and systematically, by Dr. G. Mayr (this paper occupies some hundred pages).—Muscorum species nova, by J. Juratzka.—Symbolse ad pteridographiam et Characeas Hungariæ præcipue Banatus, by Dr. V. de Borbás.—On some Lepidoptera, by A. F. Rogenhofer.—Researches made upon leaf galls and their causes on Vitis vinifera, by G. von Haimhoffen.— Six years' observations on the first appearances both in the animal and vegetable kingdoms at New Cologne near Milwaukee (North America), by Th. A. Bruhin.—On the flora of Lower Austria (second paper), by J. Wiesbaur.