Introduction

The common shrew, a small insectivorous mammal, has a remarkable karyotypic variation. Its diploid number of chromosomes varies from 2n = 20 to 2n = 33 due to structural rearrangements, such as Robertsonian fusions and/or fissions (Rb) of 10 single-armed autosomes (g, h, i, k, m, n, o, p, q, and r), constituting the variable part of a karyotype. Four pairs of bi-armed chromosomes—af, bc, jl, and tu—and the sex chromosomes (XX in females and XY1Y2 in males) do not vary (Searle 1988; Wójcik and Searle 1988; Wójcik 1993). Following the standard nomenclature, each chromosomal arm in the common shrew karyotype is denoted by a lowercase letter of the Latin alphabet (a–u) according to their size, with a being the largest (Searle et al. 1991, 2010). The chromosome arms g-r can be represented as acrocentrics or can fuse in various combinations to form diagnostic metacentrics in a karyotype (Searle and Wojcik 1998; Wójcik et al. 2003). A specific feature of this species is its geographically contiguous distribution of individuals with similar karyotypes; groups of local populations with the same karyotypes are called “chromosomal races” (Hausser et al. 1994). At least 77 races are known within the species range (White et al. 2010; Shchipanov and Pavlova 2016, 2017; Pavlova et al. 2017); however, there are several poorly studied areas in which one could expect new races.

The initial stages of karyotype evolution in the common shrew apparently resulted from the Rb fusions of diagnostic acrocentrics, whereas whole-arm reciprocal translocations (WARTs) could have affected further amplification of diversity of fully metacentric chromosomal races (Searle and Wojcik 1998; White et al. 2010). WARTs result in the appearance of new karyotypes with at least two different pairs of diagnostic metacentrics. This disparity induces the formation of a complex meiotic configuration, a ring-of-four (RIV), in hybrids between races that differ by a single WART. The standard width of hybrid zones in which parental races produce hybrids with RIV is significantly lower compared with races with less complex hybrids, indicating a restriction of gene flow between races (Bulatova et al. 2011). Thus, the WART could be regarded as a mutation that mediates the primary isolation of karyotypically distinct forms. Although the WART is a rarely detected rearrangement, evidence of this translocation has been reported in several interracial hybrid zones (Fedyk and Chętnicki 2009; Pavlova and Bulatova 2010; Bulatova et al. 2011).

It has been assumed that WARTs had a significant function in the evolution of a number of Scandinavian races, suggesting a chain of the transformation of karyotypes (Halkka et al. 1987). Based on the general logic of WARTs, a karyotype that had been predicted as an intermediate link in the chain was found (Polyakov et al. 1997). It was shown that the relationship in a chain of Uralian races resulted from consecutive WARTs and that this transformation chain linked the Siberian race Novosibirsk and Scandinavian races in Finland (Polyakov et al. 2000, 2001).

The karyotypic diversity of the common shrew in the Russian component of the species’ area resulted principally from WARTs; we have suggested that the 27 races that are distributed throughout Russia can be arranged into at least four “karyotypic chains” (Shchipanov and Pavlova 2017). In these chains, there are two gaps in which a new karyotype is required. In particular, one gap lies in a chain in which the Sok race is the basal race. The “Sok” chain includes the Petchora race, which possesses the metacentric gi, which is unique to the common shrew. This chromosome exists only in the Sorex antinorii karyotype, a closely related species that inhabits in the Alps. White et al. (2010) hypothesized the occurrence of an intermediate karyotype that directly links the adjoining Petchora and Sok races by a single translocation.

These findings prompted us to study the karyotypic diversity of the common shrew in a poorly studied area between the estuary of the Pechora River and the Northern Ural Mountains, where such new karyotypes could be found. In this report, we present new data on the karyotypic variation of common shrews from this area.

Material and methods

Animals were collected from several localities in the Komi Republic in August 2016 and in the vicinities of the town of Naryan-Mar, Nenets Autonomous Okrug, in July 2017 (Fig. 1). The shrews were caught following our trapping protocol (Shchipanov et al. 2000, 2005). Animals were processed during a day of capture. Before that, the animals were maintained in separate cages with ad libitum access to food and water. The animals were sacrificed under ether anesthesia. No special permission for use of shrews in cytogenetic researches is required in the Russian Federation.

Fig. 1
figure 1

Map of the distribution of known chromosomal races (pale gray areas) and localization of new karyotypic variants of the common shrew in the study area. Kn, the Kanin; Kr, the Kirillov; Pt, the Petchora; Ma, the Manturovo; So, the Sok; and Se, the Serov races. Five-beam stars indicate localization of known hybrid zones. New localities of the Serov race are marked as four-beam stars; white ring: “Inta” variant; black ring: “Naryan-Mar” variant; and an eight-beam star: recombinant karyotype. The localities are numbered as in Table 1

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In total, six common shrews were karyotyped from the Komi Republic and two shrews from Nenets Okrug by a standard mitotic technique from both bone marrow and spleen (Bulatova et al. 2009). The trypsin–Giemsa staining technique of Král and Radjabli (1974) was used for the identification of each chromosome arm by G-bands. The racial status is defined in correspondence to the standard nomenclature (Searle et al. 2010).

Results and discussion

Four karyotypic variants were determined among the shrews that we studied (Table 1). All individuals had NFa = 18, whereas the diploid number of chromosomes was 20 in females and 2n = 21 in males. Shrews from localities 1–3 with the karyotype go, hn, ip, km, and qr belonged to the Serov race. No polymorphic karyotypes of the Serov race were found. These new data expand the inhabited area of the Serov race to the Northern Urals, which lies approximately 500 km north of the known margin. This race belongs to the “karyotypic chain” of related karyotypes, with the Sok race as a basal race (Shchipanov and Pavlova 2017).

Table 1 Karyotypic variants of the common shrew found in the studied area. Only diagnostic chromosomes are indicated. Male (m) and female (f)
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One female from locality 3 in the vicinity of the town of Inta had a new set of diagnostic metacentrics in a karyotype—go, hn, im, kq, and pr—which we named the “Inta” variant (Fig. 2a). This karyotype corresponds entirely to the previously suggested intermediate karyotype that links the karyotypes of the Petchora and Sok races (White et al. 2010). Although the “Inta” karyotype was identified in the same locality as the pure Serov race, we did not find any hybrids between them. Considering that the animal that was studied had a homozygous karyotype, we propose that it belongs to a new chromosomal race (“Inta”).

Fig. 2
figure 2

G-banded karyotypes of the common shrew: a “Inta” variant; b “Naryan-Mar” variant, and c recombinant karyotype

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An individual from locality 4 in the vicinity of the town of Naryan-Mar had the chromosomes go, hn, im, kr, and pq (Fig. 2b). Its karyotype differed from the “Inta” variant by two metacentric chromosomes, kr and pq, which can originate by a single WART between kq and pr metacentrics in the “Inta” karyotype. This homozygous karyotype suggests the existence of another new race (“Naryan-Mar”). As a result, the chain of WART transformations that links the races in the region forms a tree-like structure (Fig. 3).

Fig. 3
figure 3

The sequence of transformations of racial karyotypes in the “Sok” karyotypic chain by consecutive WARTs. Arrows indicate the translocations of chromosomal arms between diagnostic metacentrics

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The animal from locality 5 had a karyotype that was determined to be a heterozygote: gi, hn, mo, kq-kr-pr-pq (Fig. 2c). Apparently, this karyotype is a recombinant that resulted from hybridization between the Petchora race and “Naryan-Mar” karyotypic variant. A hypothetical F1 hybrid between them with the metacentrics gi-go, hn, mo-mi, kq-kr-pr-pq can produce eight types of gametes—in particular, gi, hn, mo, kr, pq and gi, hn, mo, pr, kq. When such individuals hybridize, offspring with gi, hn, mo, kq-kr-pr-pq chromosomes can be produced. We attribute the appearance of such recombinants to the occurrence of small local populations at the periphery of the racial ranges.

At the northern periphery of the species range, we observed scattered patches of favorable habitats that were surrounded by the vast area that is available for the common shrew only temporarily. The recombinant karyotype was found in a small meadow that was surrounded by lichen tundra, from which common shrews were absent. We hypothesized that such small populations could be composed from individuals of different races within a contact zone and existed temporally as a local hybrid population.

We believe that the existence of local hybrid populations is significant in understanding the origin and fixation of new chromosomes. According to our data (Shchipanov and Pavlova 2017, Appendix), over 95% of the 911 karyotypes were polymorphic in the nearest (± 25 km from the center) vicinities of hybrid zones, whereas within the racial ranges, the polymorphic karyotypes constituted only 7% of 832 animals. We concluded that the northern periphery of the inhabited area of the common shrew in European Russia warrants further study with regard to karyotype diversity.