N. A. Formozov

A Molecular Genetic Study of Hybridization in Four Species of Ground Squirrels (Spermophilus: Rodentia, Sciuridae)

Four species of ground squirrel—yellow (Spermophilus fulvus), russet (S. major), small (S. pygmaeus), and spotted (S. suslicus)—occur in the Volga region. Between S. major and S. pigmaeus, S. major and S. fulvus, and S. major and S. suslicus, sporadic hybridization was reported. Using sequencing and restriction analysis, we have examined the mtDNA C region in 13 yellow, 60 russet, 61 small, 45 spotted ground squirrels, and 9 phenotypic hybrids between these species. It was shown that 43% of S. major individuals had “alien” mitotypes typical of S. fulvus and S. pygmaeus. Alien mitotypes occurred both within and outside sympatric zones. No alien mitotypes were found in 119 animals of the other three species, which suggests that only one parental species (S. major) predominantly participates in backcrosses. Phenotypic hybrids S. fulvus × S. major and S. major × S. pygmaeus) were reliably identified using RAPD–PCR of nuclear DNA. However, we could find no significant traces of hybridization in S. major with alien mitotypes. Analysis of p53 pseudogenes of S. major and S. fulvus that were for the first time described in the present study produced similar results: 59 out of 60 individuals of S. major (including S. major with S. fulvus mitotypes) had only the pseudogene variant specific for S. major. This situation is possible even at low hybridization frequencies (less than 1% according to field observations and 1.4 to 2.7% according to nuclear DNA analysis) if dispersal of S. major from the sympatric zones mainly involved animals that obtained alien mtDNA via backcrossing. The prevalence of animals with alien mitotypes in some S. major populations can be explained by the founder effect. Further studies based on large samples are required for clarifying the discrepancies between mitochondrial and nuclear DNA data.

A Search for Y-Chromosomal Species-Specific Markers and Their Use for Hybridization Analysis in Ground Squirrels ( Spermophilus : Rodentia, Sciuridae)

In four ground squirrel species from the Volga region—yellow (Spermophilus fulvus), russet (S. major), little (S. pygmaeus), and speckled (S. suslicus)—four hybridization variants (major/fulvus, major/pygmaeus, major/suslicus, and pygmaeus/suslicus) have been reliably described. Earlier we have shown that populations of S. major from the Volga region were characterized by wide introgression of mtDNA from S. fulvus and S. pygmaeus, which probably, resulted from ancient hybridization [5]. In this study, the same populations were used to analyze the introgression of the Y chromosome, which (unlike mtDNA) is paternally inherited. Three genes, ZfY, SRY, and SmcY were tested as Y-chromosomal candidate markers. It was demonstrated that Y chromosome of ground squirrels lacked the ZfY gene, while its homologous structure, ZfY(X), was presumably linked to the X chromosome. The SRY region examined was rather conservative. In particular, the sequences determined in S. major and S. fulvus were identical, while three out of four substitutions found in S. pygmaeus were located in the coding region. The SmcY gene was found to be the most suitable marker, providing distinguishing of all of the four ground squirrel species by nine nucleotide substitutions. Introgression at the Y chromosome was observed only in two cases: in one S. major individual (out of 51 phenotypically pure animals) caught in the major/fulvus sympatry zone, and in four (one litter) out of fourteen S. fulvus individuals caught in close vicinity of the sympatry zone of these two species. Among 28 S. pymaeus and 9 S. suslicus individuals, no foreign SmcY genes were detected. Two colonies of the “hybrid swarm” type were examined with eight major/suslicus hybrids analyzed in the first and seventeen major/fulvus hybrids in the second colony. The prevalence of the S. major paternal lineages was observed in both colonies (87.5 and 82.4%, respectively). The data obtained suggest that compared to wide mtDNA introgression, introgression of Y chromosome in the Volga region ground squirrels is statistically significantly less frequent event.

The first genetic evidence of hybridization between West European and Northern white-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow region

The complex genetic examination of hedgehogs from the vicinity of the village of Nikolina Gora (Moscow region, Odintsovskii district) showed both Erinaceus europaeus and E. roumanicus in the sample. One of the hedgehogs was designated as E. roumanicus by the nucleotide sequence of 1 TTR intron but possessed mitochondrial DNA of E. europeus. Only one of the chromosomal pairs that differ in E. europeus and E. roumanicu s was heteromorphic in this specimen. Its hybridous origin as the offspring of one or several backcrosses between F1 hybrid and E. roumanicus was suggested.

Nitrogen fixation as a possible physiological basis of coprophagy in pikas (Ochotona, Lagomorpha, Mammalia).

Two families of the order Lagomorpha, Ochoto� nidae, and Leporidae, are characterized by a peculiar dietary adaptation, i.e., obligate autocoprophagy. The animal produces excrement of two types: solid flat� tened pellets, which contain large undigested food

Maintaining morphological specificity and genetic introgression in populations of the great tit Parus major and the Japanese tit P. minor in the middle Amur region

The ranges of the great tit Parus major and the Japanese tit P. minor overlap in the middle Amur region, where hybridization of these two species occur. These species have contacted for nearly a century on the western slope of the Malyi Khingan Ridge (the central part of the sympatry zone), but the great tit has colonized territories to the east of the ridge only in the last two decades. The percentage of the P. minor’s allele of intron 2 of the mioglobin gene has significantly increased from 8.9% in the west to 27.8% in the east in phenotypically major’s populations. Thus, the percentage of foreign mtDNA in P. major populations did not change significantly from west (6.2%, n = 120) to east (3.2%, n = 61). Simultaneous use of two genetic markers (one nuclear and the other mitochondrial) supports our conclusion on strong introgression in the populations of both species, which nevertheless maintain their morphological specificity in the contact zone.

Reduction of plant fibers in the digestive tract of two pika species (Ochotona pallasi and O. dauurica, Lagomorpha, Ochotonidae)

The distribution of fibers of different sizes in the gastrointestinal tract in two species of pikas—Pallas’ pika Ochotona pallasi and daurian pika O. dauurica—was studied. It was established that fibers of small-sized fractions dominated in all organs of the digestive tract of both pika species, the proportion of which in the stomach proved to be even higher than in fine-grinding voles. No distinct changes in the composition of the size fractions of fibers from organ to organ were observed in the studied individuals of both species, which may be due to frequent consumption of finely dispersed cecotrophs by pikas, which enrich the primary chewed food with small fibers.

The structure of the epithelial surface of the gastrointestinal tract of Pikas (Ochotona pallasi and O. dauurica, Lagomorpha, Ochotonidae): Functional and species specificity

The macro- and microrelief of the surface of the digestive tract mucosa of two pika species—Pallas’s (Ochotona pallasi) and Daurian (O. dauurica)—were studied in detail using whole-mount preparations and scanning electron microscopy. The structural features of the intestinal mucosal surface specific of mammals, such as the formation of projections on the crest of the cecal spiral fold and microcells in the colonic ampulla, were studied. It was found that the colonic mucosa forms sparse large conical villi in pocket cavities and on the surface of muscle bands. Significant differences in the cecal mucosal relief were found between the species studied. The possible functional significance of the identified morphological features is discussed.

The history of ranges of the great tit (Parus major) and Japanese tit (Parus minor) in the Amur Region

AbstractsThe history of ranges of the great tit (Parus major) and Japanese tit (P. minor) in the Amur River basin is described on the basis of original data collected between 1970 and 2010 and published data. The main factor accounting for the expansion of the great and Japanese tits to the Amur basin and neighboring territories in the 19th to 21st centuries is economic activity, primarily agriculture and timber harvesting. The approximate range boundaries and the sympatry zone of these two species have been determined for the second half of the 19th century; the beginning, middle, and third quarter of the 20th century; and the turn of the 21st century. Three different ecological channels consecutively played the main role in the eastward expansion of the great tit: the Amur River valley (from the mid-19th to the early 20th century), the Trans-Siberian Railroad (since the early 20th century), and the Baikal-Amur Railroad (since the 1970s). It is shown that the concept concerning the finding of great tits in Udskii Ostrog by Middendorff’s expedition is erroneous: according to dates on the labels, the corresponding two specimens were in fact collected in a different geographic locality. It has been found that Komsomolsk-on-Amur is a new locality jointly inhabited by both species, independent of the main zone of their sympatry. It has appeared very recently, at the turn of the 21st century.

Song Variability in Pied Flycatchers Ficedula hypoleuca: Impact of the Sympatry with Collared Flycatchers F. albicollis

Abstract. In the sympatry zone many Pied Flycatcher males perform songs that resemble those of a sibling species (Collared Flycatcher): these are so-called mixed songs. The higher abundance of the Collared Flycatcher was once considered a possible cause of mixed singing. To examine this hypothesis we studied the influence of the Collared Flycatcher on the interpopulational song variability in the Pied Flycatcher in four areas with different abundances of Collared Flycatchers. We focused on: 1) the abundance of mixed singers and their distribution; 2) geographical variations of typical Pied Flycatcher songs. We show for the first time that mixed singing in the Pied Flycatcher is common also when its abundance is as high as and higher than that of the Collared Flycatcher. In the old area of sympatry about 40% of all Pied Flycatcher males had Collared-Flycatcher-like syllables in their repertoire. At the same time, the habitat distribution of mixed singers matches that of the Collared Flycatcher. In the context of our data we propose a hypothesis of mixed song-formation. We have also demonstrated interpopulational variability in pure Pied Flycatcher songs, with species-specific differences being more pronounced in sympatric populations than in allopatric ones. This pattern is in agreement with the theory of character displacement and acoustic divergence in a sympatry zone, but the differences discovered in pure vocalizations are evidently not the result of interactions with the sibling species.

The intraspecies variability of Spermophilus relictus sensu lato Kaschkarov 1923 (Sciuridae, Rodentia)

The intraspecies variability of Spermophilus relictus sensu lato was studied based on 27 measurements of skulls from 67 specimens of relict ground squirrels (S. relictus) and 66 specimens of Tien Shan ground squirrels (S. ralli), as well as six specimens of the relict ground squirrel from the Gissar Ridge (Tien Shan). A colorimetric analysis of skins of relict ground squirrels (19 specimens, including three individuals from the Gissar Ridge) and Tien Shan ground squirrels (19 specimens) was made. Significant intraspecies variability was found in the relict and Issyk-Kul ground squirrels, whereas the interspecies differences were small, raising questions about the species independence of the Tien Shan ground squirrel (S. ralli).