Research Article |
Corresponding author: Tereza Holicová ( holic.ter@seznam.cz ) Academic editor: Raquel López-Antoñanzas
© 2018 Tereza Holicová, František Sedláček, Anna Mácová, Jakub Vlček, Jan Robovský.
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:
Holicová T, Sedláček F, Mácová A, Vlček J, Robovský J (2018) New record of Microtus mystacinus in eastern Kazakhstan: phylogeographical considerations. ZooKeys 781: 67-80. https://doi.org/10.3897/zookeys.781.25359
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The Eastern European vole (Microtus mystacinus) is an arvicoline rodent distributed across northern and eastern Europe, the Balkans, Turkey, Armenia, NW and N Iran, Russia as far east as the Tobol River in W Siberia, and W and N Kazakhstan. We present a novel records from eastern Kazakhstan (the village of Dzhambul – 49°14'21.3"N, 86°18'29.9"E and the village of Sekisovka – 50°21'9.18"N, 82°35'46.5"E) based on mtDNA and we discuss implications of this findings on biogeography of eastern Kazakhstan populations. Marine Isotope Stage 11 is considered an important period for the diversification of the arvalis species group. In the context of our study, it is important to analyse genetically discontinuous Siberian populations, and the current distribution of Microtus mystacinus in new localities in eastern Kazakhstan.
Microtus mystacinus , Kazakhstan
The Eastern European vole, Microtus mystacinus De Filippi, 1865, is an arvicoline rodent with an unsettled nomenclature. It has been named most commonly as M. subarvalis Meyer, Orlov & Skholl, 1972, Microtus epiroticus Ondrias, 1966, Microtus rossiaemeridionalis Ognev, 1924, and Microtus levis Miller, 1908 (e.g.,
In general, Microtus mystacinus represents one of the best cases of a cryptic species in arvicolines, because it was primarily recognized by chromosomal number (Microtus mystacinus: 2n = 54; Microtus arvalis: 2n = 46) (
The distribution and habitat preferences of the Eastern European vole are relatively well known due to the intensive attention devoted to it (see
Populations occupying the Artic Svalbard Archipelago (
When considering the distribution of Microtus mystacinus within Kazakhstan, there are records from the western or north-western parts. The easternmost record is from the Karabalyk district (
A survey of small mammals conducted in eastern Kazakhstan provided the surprising discovery of three specimens of Microtus mystacinus, that are characterized here based on molecular methods. The first sample (Kazakhstan 1) was collected in July 2006 on pasture land near the village of Dzhambul (GPS coordinates: 49°14'21.3"N, 86°18'29.9"E) by FS and two more specimens (Kazakhstan 2, 3) were collected in September 2017 near a pond not far from the village Sekisovka (GPS coordinates: 50°21'9.18"N, 82°35'46.5"E) by AM and JV.
DNA extraction was carried out using the Genomic DNA Mini Kit – tissue (Geneaid, New Taipei, Taiwan). We amplified the mitochondrial gene cytochrome b (cyt b hereinafter) using universal primers L14724, L15162, H15149 and H15915 (
We obtained 1137 base pairs long sequences that satisfied the quality of base pairs (GenBank access number LT970847-LT970849). These were compared using available sequences from GenBank, specifically with 250 specimens that comprise all available sequences of Microtus mystacinus (under names Microtus levis, M. rossiameridionalis and Microtus mystacinus), and representative sequences of particular clades in Microtus arvalis and M. obscurus associated with previous studies (
Some analyses were applied for Microtus mystacinus only. Specifically, haplotype characteristics were identified using DnaSP version 5.0 (
The obtained sequences of 1137 base pairs from three specimens exhibited close relationships with available cyt b sequences of Microtus mystacinus, in all comparisons. Specifically, they were nested inside this species, so our study identified this species in eastern Kazakhstan (see also below). All sequences of Microtus mystacinus form a sister group to the Microtus obscurus + Microtus arvalis, in accordance with previous comprehensive studies (e.g.,
Considering the intraspecific structure in Microtus mystacinus, we can distinguish two deep lineages (Iran, abbreviated as IR) and the rest of populations mostly from Europe, additionally divided into several sub-lineages (TU, EU, GK), concordantly in ML and BI phylogenetic trees and the haplotype network (see Figure
In general, Microtus mystacinus exhibited rather low intraspecific cyt b distances (except for the Iranian subset) and the obtained interspecific cyt b distances (see Table
The K2P Inter – and intra-species average estimates of K2 genetic distance for cyt b in recognized lineages of Microtus mystacinus (TU – Turkey, Armenia; EU – Europe; GK – Greece, Kazakhstan; IR – Iran).
1. | 2. | 3. | 4. | 5. | 6. | 7. | 8. | 9. | 10. | |
---|---|---|---|---|---|---|---|---|---|---|
1. TU | 0.007 | |||||||||
2. EU | 0.025 | 0.007 | ||||||||
3. GR | 0.021 | 0.016 | 0.006 | |||||||
4. Armenia_1 | 0.024 | 0.019 | × | × | ||||||
5. Greece | 0.016 | 0.011 | × | 0.009 | 0.001 | |||||
6. Kazakhstan | 0.023 | 0.018 | × | 0.007 | 0.008 | 0.006 | ||||
7. IR | 0.035 | 0.044 | 0.031 | 0.031 | 0.034 | 0.028 | 0.013 | |||
8. M. obscurus | 0.067 | 0.066 | 0.065 | 0.062 | 0.066 | 0.059 | 0.068 | 0.028 | ||
9. Microtus arvalis | 0.067 | 0.057 | 0.065 | 0.062 | 0.066 | 0.063 | 0.067 | 0.059 | 0.003 | |
10. M. transcaspicus | 0.075 | 0.079 | 0.071 | 0.069 | 0.072 | 0.065 | 0.068 | 0.067 | 0.084 | 0.004 |
The estimated clade divergence times varied substantially according to the calibration used (see Table
Time to the most recent common ancestor (TMRCA and 95% HPD lower/upper limit – in million years) with BEAST2 for particular Microtus species (T – M. transcaspicus, M – Microtus mystacinus. O – M. obscurus. A – Microtus arvalis) and recognized lineages of Microtus levis (TU – Turkey, Armenia; EU – Europe; GK – Greece, Kazakhstan; IR – Iran).
Nodes | Analysis 1 – fossil calibrations |
|
|
|
TMRCA | 95% HPD | TMRCA (95%HPD) | TMRCA (95%HPD) | |
a. T+M+O+A | 1.102 | 0.77–1.28 | 0.238 (0.16–0.35) | – |
b. M+O+A | 0.797 | 0.60–1.05 | 0.217 (0.15–0.31) | 0.531 (0.42–0.67) |
c. O+A | 0.616 | 0.51–0.78 | 0.184 (0.12–0.26) | 0.478 (0.40–0.56) |
d. T | 0.537 | 0.32–0.57 | 0.040 (0.01–0.08) | - |
e. O | 0.410 | 0.27–0.58 | 0.119 (0.07–0.18) | 0.173 (0.10–0.29) |
f. A | 0.490 | 0.48–0.54 | 0.146 (0.10–0.21) | 0.446 (0.39–0.49) |
g. IR+ EU+GK+TU | 0.575 | 0.04–0.77 | 0.147 (0.09–0.22) | 0.033 (0.00–0.08) |
h. EU+GK+TU | 0.408 | 0.28–0.57 | 0.092 (0.05–0.14) | – |
i. EU+GK | 0.332 | 0.23–0.47 | – | – |
j. TU | 0.235 | 0.10–0.40 | 0.022 (0.01–0.04) | – |
k. EU | 0.219 | 0.14–0.32 | 0.075 (0.05–0.11) | – |
l. GK | 0.280 | 0.19–0.40 | – | – |
m. IR | 0.390 | 0.24–0.47 | 0.117 (0.06–0.18) | – |
Evolution and diversification of arvicoline rodents, including the arvalis-group, has been closely related to Quaternary climatic oscillations and the associated abiotic and biotic environmental factors (e.g.,
In our data, we observed synchronous, deep intraspecific divergences in all three species around 0.49–0.41 Mya (see Figure
To conclude, our study proved an additional occurrence of Microtus mystacinus in Kazakhstan. The studies of
The distribution of Microtus mystacinus could be partly human-induced, as documented by
Our study is the first genotyping of Microtus mystacinus from the eastern part of its distribution, where its’ occurrence is more discontinuous. In the context of our study, it is important to analyse genetically these Baikal and Far Eastern populations, and further map out the extent of Microtus mystacinus occurrence in East Kazakhstan.
We would like to thank Professor Jan Zrzavý for financial support; AM and JV were supported by grant number 31-17-19831S. We also would like to express our gratitude to Joel James Brown and Nathalie Yonow for professional language editing and to the editor and reviewers for their very valuable comments which helped to improve our manuscript.