Research Article |
Corresponding author: Iryna A. Kryshchuk ( drigka@list.ru ) Academic editor: Svetlana Galkina
© 2021 Iryna A. Kryshchuk, Victor N. Orlov, Elena V. Cherepanova, Yuri M. Borisov.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kryshchuk IA, Orlov VN, Cherepanova EV, Borisov YM (2021) Unusual chromosomal polymorphism of the common shrew, Sorex araneus L., in southern Belarus. Comparative Cytogenetics 15(2): 159-169. https://doi.org/10.3897/CompCytogen.v15.i2.63084
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Analysis of the frequency of karyotypes and chromosomal rearrangements in the distributional ranges of four metacentric races of Sorex araneus Linnaeus, 1758 has revealed features that are not typical for polymorphic populations of this species. The frequency of the acrocentric karyotype and heterozygotes for fusion of acrocentric chromosomes turned out to be significantly higher than expected in case of random crossing. As an explanation for the unusual polymorphism, it has been suggested that metacentric races may hybridize with acrocentric populations that remained from the ancient chromosomal form.
Acrocentric morph, chromosomal race, Hardy-Weinberg ratio, dihybrid and trihybrid segregation
The polymorphic part of the karyotype of the common shrew, Sorex araneus Linnaeus, 1758, is represented by 12 pairs of acrocentric chromosomes (g, h, i, j, k, l, m, n, o, p, q, and r) that have a capacity to form new arm combinations in metacentric chromosomes. The recognition, naming, and systematics of populations with different karyotypes has long been an important issue in the common shrew (
Three races of the common shrew with race-specific metacentrics, West Dvina (gm, hk, ip, no, qr), Białowieża (g/r, h/n, ik, m/p), and Kiev (g/m, hi, k/o) races, have been previously described near the northern, western, and southern borders of Belarus (
A Collection sites and distribution of chromosomal races Sorex araneus races in Belarus. Short abbreviations of races and their numbers indicate samples according to previously published (
Two hypotheses of the origin of chromosomal polymorphism in populations of the common shrew in Belarus were proposed and discussed (
To investigate the causes of chromosomal polymorphism in the common shrew in southern Belarus, we collected additional samples in peripheral parts of the ranges of four chromosomal races (Fig.
The study area is a mosaic of forest and meadow biotopes. Animals were captured in 11 sites in the area between the Berezina, Ptich, and Pripyat rivers (Gomel and Mogilev regions) in July–September, 2017–2018 (Fig.
Collection sites, karyotypes of the individual common shrews, and polymorphic chromosome races in the southern Belarus. In the karyotype characteristics, only the variable autosomal arms are included (g–r). These arms can be presented in a dissociated state as individual acrocentric autosomes (e.g. h, i, k, o) or as components of metacentric autosomes (e.g. hi, ko). The presence of heterozygous karyotypes is indicated by a slash between the two arms, e.g. h/i, k/o (follows
No. | Collection site | Latitude, Longitude | Short abbreviation of races | 2NA | Karyotype | Number of shrews | |
---|---|---|---|---|---|---|---|
New data |
|
||||||
Polymorphic Svetlogorsk (Sv) race (h/i, k/o) | |||||||
1 | Parichi | 52°48'04"N, 29°25'58"E | Sv | 28 | g, h, i, k, m, n, o, p, q, r | – | 3 |
Sv | 26 | g, h/i, k/o, m, n, p, q, r | – | 9 | |||
Sv | – | (12) | |||||
2 | Zhlobin | 52°50'32"N, 29°45'35"E | Sv | 28 | g, h, i, k, m, n, o, p, q, r | – | 1 |
Sv | 26 | g, h/i, k/o, m, n, p, q, r | – | 8 | |||
– | (9) | ||||||
Polymorphic Oktiabrskiy (Ok) race (h/n, i/k) | |||||||
3 | Lyubonichi | 53°15’19N, 29°10’21E | Ok | 28 | g, h, i, k, m, n, o, p, q, | 2 | 2 |
Ok | 25 | g, hn, i/k, m, o, p, q, r | 4 | 2 | |||
Ok | 25 | g, h/n, ik, m, o, p, q, r | 1 | 2 | |||
Ok | 26 | g, h/n, i/k, m, o, p, q, r | 3 | 5 | |||
Ok | 27 | g, h/n, i, k, m, o, p, q, r | 2 | 1 | |||
Ok | 27 | g, h, i/k, m, n, o, p, q, r | 3 | – | |||
Ok | (15) | (12) | |||||
4 | Rozhanov Oktiabrskiy | 52°35'51"N, 28°45'08"E | Ok | 28 | g, h, i, k, m, n, o, p, q, r | 5 | 3 |
Ok | 26 | g, h/n, i/k, m, o, p, q, r | 19 | 3 | |||
H | 25 | g, h/n, i, ko, m, p, q, r | 2 | – | |||
(26) | (6) | ||||||
5 | Zatishie (Oktiabrskiy) | 52°34'26"N, 28°44'37"E | Ok | 28 | g, h, i, k, m, n, o, p, q, r | 2 | – |
Ok | 26 | g, h/n, i/k, m, o, p, q, r | 15 | – | |||
Sv | 26 | g, hi, k, m, n, o, p, q, r | 1 | 2 | |||
(18) | (2) | ||||||
6 | Luchicy | 52°27'16"N, 28°48'35"E | Ok | 28 | g, h, i, k, m, n, o, p, q, r | 4 | 2 |
Ok | 26 | g, h/n, i/k, m, o, p, q, r | 8 | – | |||
Bs | 27 | g, h/k, i, m, n, o, p, q, r | 1 | 1 | |||
(13) | (3) | ||||||
7 | Konkovichi | 52°9'22"N, 28°43'30"E | Ok | 28 | g, h, i, k, m, n, o, p, q, r | 6 | 4 |
Ok | 26 | g, h/n, i/k, m, o, p, q, r | 21 | 2 | |||
Ok | 25 | g, hn, i/k, m, o, p, q, r | 7 | – | |||
Ok | 24 | g, hn, ik, m, o, p, q, r | 9 | – | |||
Bs | 27 | g, h/k, i, m, n, o, p, q, r | – | 1 | |||
(43) | (7) | ||||||
8 | Borki | 52°05'50"N, 27°49'19"E | Ok | 28 | g, h, i, k, m, n, o, p, q, r | – | 1 |
Ok | 25 | g, r, hn, i/k, m, o, p, q | – | 1 | |||
Ok | 27 | g, m, h/n, i, k, o, p, q, r | – | 1 | |||
Ok | 27 | g, r, h, n, i/k, m, o, p, q | – | 1 | |||
– | (4) | ||||||
Polymorphic Białowieża (Bi) race ([gr or mp], hn, ik) | |||||||
9 | Turov | 52°04'15"N, 27°45'48"E | Bi | 28 | g, h, i, k, m, n, o, p, q, r | – | 4 |
Bi | 25 | g, h/n, i/k, m/p, o, q, r | 27 | 1 | |||
H | 26 | g, h, ik/ko, m, n, p, q, r | – | 1 | |||
Bs | 27 | g, h/k, i, m, n, o, p, q, r | 2 | 2 | |||
(30) | (7) | ||||||
10 | Khvoyensk | 52°2'11"N, 27°56'40"E | Bi | 28 | g, h, i, k, m, n, o, p, q, r | 10 | – |
Bi | 25 | g/r, h/n, i/k, m, o, p, q | 8 | 10 | |||
Bi | 25 | g, hn, i/k, m, o, p, q, r | 3 | 3 | |||
Bi | 26 | g, h/n, i/k, m, o, p, q, r | 1 | 3 | |||
Bi | 24 | g, hn, ik, m, o, p, q, r | 1 | 2 | |||
H | 26 | g, h/n, k/o, m, i, p, q, r | 2 | – | |||
Bs | 27 | g, h/k, i, m, n, o, p, q, r | 2 | – | |||
(27) | (18) | ||||||
Polymorphic Kiev (Ki) race (g/m, h/i, k/o) | |||||||
11 | Skrygalov | 52°03'20"N, 28°49'10"E | Ki | 28 | g, h, i, k, m, n, o, p, q, r | 1 | – |
Ki | 25 | g/m, h/i, k/o, n, p, q, r | 25 | – | |||
H | 26 | g, h, ik/ko, m, n, p, q, r | 1 | – | |||
(27) | – | ||||||
199 | 80 |
Chromosome mounts were prepared from bone marrow and spleen cells after a routine technique with colchicine treatment (
For statistical procedures, we proceeded from a single, two- and three- locus model with a codominant type of inheritance. The calculations were based on the matrix of individual karyotypes (Table
According to the principles of Mendelian inheritance, nine different karyotypes are theoretically possible in polymorphic populations of the Oktiabrskiy or Svetlogorsk races (dihybrid segregation): (hn, ik), (hn, i, k), (h, n, ik), (h, n, i, k), (hn, i/k), (h, n, i/k), (h/n, ik), (h/n, i, k), and (h/n, i/k). In the case of a random combination of gametes and the absence of selection, the expected frequencies of genotypes (e. g. karyotypes) are constant, their values are given in genetic reference books. The expected frequency of the acrocentric (h, n, i, k) and homozygous (hn, ik) karyotypes should be 1/16 (0.0625), and heterozygous one (h/n, i/k) – ¼ (0.25). Similarly, in populations polymorphic by three metacentrics (Białowieża and Kiev races), 27 genotypes are theoretically possible (trihybrid segregation). The expected frequency of the acrocentric ([g, r or m, p] h, n, i, k) and homozygous ([gr or mp], hn, ik) karyotypes should be 1/64 (0.0156), and heterozygous one ([g/r or m/p], h/n, i/k) – 1/8 (0.125).
The expected frequency of homozygotes and heterozygotes was estimated by the Hardy–Weinberg equation: p2+2pq+q2=1, where p2 is the proportion of homozygotes for one of the alleles (e. g. hn), p is the frequency of this allele, 2pq is the proportion of heterozygotes (h/n), q2 is the proportion of homozygotes for the alternative allele (h, n), and q is the frequency of the corresponding allele. We used a variant of the Hardy–Weinberg equation for small samples (
The distribution of the four chromosomal races in southern Belarus is shown in Fig.
We found rare hybrids of the Białowieża and Kiev races (recombinants h/n, k/o and complex heterozygotes ik/ko) in two localities of the Białowieża race distribution and in one locality inhabited by the Kiev race along the southern bank of the Pripyat river (Fig.
The studied samples allowed us to compare the observed and expected frequencies of three karyotypes (morphs) in each chromosomal race, including acrocentric karyotype, homozygous and heterozygous metacentric karyotypes in four races (Tables
The frequency of karyotypes recorded in studied localities of the Oktiabrskiy and Svetlogorsk races; O – observed frequency, E – expected frequency (after Table
Number of shrews | Karyotypes | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Acrocentric | Heterozygous | Homozygous | Heterozygous | Homozygous | |||||||||||
(Ok) h, n, i, k or (Sv) h, i, k, o | h/n, i/k | hn, ik | h/i, k/o | hi, ko | |||||||||||
O | E | χ2 | O | E | χ2 | O | E | χ2 | O | E | χ2 | O | E | χ2 | |
Oktiabrskiy race (Ok) | |||||||||||||||
141 | 31 | 8.7 | 57.2 | 68 | 35.2 | 30.6 | 9 | 8.7 | NS | – | – | – | – | – | – |
0.220 | 0.062 | *** | 0.482 | 0.250 | *** | 0.064 | 0.062 | ||||||||
Svetlogorsk race (Sv) | |||||||||||||||
21 | 4 | 1.3 | 5.6 | – | – | – | – | – | – | 17 | 5.2 | 26.8 | – | 1.3 | – |
0.190 | 0.062 | * | 0.809 | 0.250 | *** | 0.062 |
G-banded karyotypes of the acrocentric morph of the common shrew (male) from Konkovichi, Oktiabrskiy race.
Not only the observed frequency of karyotypes with heterozygotes, but also the frequency of heterozygotes for fusion of acrocentric chromosomes significantly exceeded the expected by Hardy-Weinberg, while the observed frequency of homozygotes is less than expected (Table
The frequency of karyotypes recorded in studied localities of the Białowieża and Kiev races; O – observed frequency, E – expected frequency (after Table
Number of Shrews | Karyotypes | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Acrocentric | Heterozygous | Homozygous | Heterozygous | Homozygous | |||||||||||
(Bi) g, r, m, p, h, n, i, k or (Ki) g, m, h, i, k, o | [g/r or m/p] h/n, i/k | [gr or mp], hn, ik | g/m, h/i, k/o | gm, hi, ko | |||||||||||
O | E | χ2 | O | E | χ2 | O | E | χ2 | O | E | χ2 | O | E | χ2 | |
Białowieża race (Bi) | |||||||||||||||
73 | 14 | 1.1 | 151.2 | 46 | 9.1 | 830 | – | 1.1 | – | – | – | – | – | – | – |
0.192 | 0.016 | *** | 0.630 | 0.125 | *** | 0.016 | |||||||||
Kiev race (Ki) | |||||||||||||||
26 | 1 | 1.1 | 0.009 | – | – | – | – | – | – | 25 | 3.25 | 9.9 | – | 1.1 | |
0.038 | 0.016 | NS | 0.961 | 0.125 | *** | 0.016 |
Tests for deviation from the Hardy–Weinberg equilibrium in the highly polymorphic samples of the Oktiabrskiy and Białowieża races; O – observed frequency, E – expected frequency.
Number of shrews | Homo-, heterozygotes | O | E | χ2 |
---|---|---|---|---|
214 | hn | 32 | 45 | 14.41 *** |
0.149 | 0.212 | |||
h/n | 133 | 106 | ||
0.622 | 0.497 | |||
h, n | 49 | 62 | ||
0.229 | 0.291 | |||
ik | 15 | 38 | 63.30 *** | |
0.070 | 0.177 | |||
i/k | 150 | 104 | ||
0.701 | 0.487 | |||
i, k | 49 | 72 | ||
0.229 | 0.335 |
The frequencies of three karyotypes (the acrocentric karyotype and karyotypes homozygous and heterozygous for metacentrics) and homozygotes and heterozygotes for fusion ik recorded in five populations of the Oktiabrskiy race (after Table
The studied polymorphic populations differ in two features from any other polymorphic populations of the common shrew:
To date, such deviations of the observed frequencies from the expected ones have not been recorded in any polymorphic populations of the common shrew. This frequency of genotypes is not typical for hybrid zones of chromosomal races of the common shrew, in particular, with an “acrocentric peak” (
In the studied hybrid zones of the common shrew, the frequency of simple heterozygotes (CIII) does not differ from that expected in the case of random crossing, and the frequency of more complex heterozygotes is constantly lower than expected even taking into account the Wahlund effect (
Therefore, the polymorphism of the studied populations is not associated with the hybridization of metacentric races (Białowieża–Kiev or Oktiabrskiy–Svetlogorsk). We may suppose that this unusual polymorphism in populations of the common shrew and the origin of the Oktiabrskiy and Svetlogorsk races is caused by the hybridization of metacentric races and the acrocentric population remained in the ancient chromosomal form. Two common shrew acrocentric populations without polymorphism were found at the southern border of the species range, in the Alps and the Balkans. These populations were described as chromosomal races Cordon (
Therefore, the fitness of the acrocentric karyotype and heterozygous metacentric karyotype may be higher than homozygous metacentric karyotypes in the studied populations. It is the increased fitness that these karyotypes became the factor responsible for the disappearance of some metacentrics, their replacement by acrocentrics, and the origin of new chromosomal races. Previously, a decrease in the frequency of race-specific metacentrics of the West Dvina race from east to west, the Białowieża race from west to east, and race-specific metacentrics of the Kiev race – from south to north in Belarus was shown (
In some populations of the peripheral parts of the Białowieża and Oktiabrskiy races, there are rare individuals that are heterozygous for the arm combination hk with karyotype g, h/k, i, m, n, o, p, q, r (Fig.
The authors are grateful to Helen S. Gaiduchenko for the assistance in capture of shrews and chromosome preparations.