Research Article |
Corresponding author: Anastasia Striuchkova ( astr2502@yandex.ru ) Academic editor: Louis Deharveng
© 2022 Anastasia Striuchkova, Irina Malykh, Mikhail Potapov, Nataliya Kuznetsova.
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:
Striuchkova A, Malykh I, Potapov M, Kuznetsova N (2022) Sympatry of genetic lineages of Parisotoma notabilis s. l. (Collembola, Isotomidae) in the East European Plain. ZooKeys 1137: 1-15. https://doi.org/10.3897/zookeys.1137.95769
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Parisotoma notabilis (Schaeffer, 1896) is one of the most abundant eurytopic species of springtails in temperate regions of the northern hemisphere, and is often used as a model species for studies on the genetics of soil microarthropod populations. Six genetic lineages (L0, L1, L2, L3, L4-Saltzwedel, L4-Hebert) are known which are distributed mainly parapatrically in Western and Central Europe. Individuals of P. notabilis from 21 locations on the East European Plain were analyzed. Three genetic lineages were found: L1, L2, L4-Hebert. In contrast to Western and Central Europe, the coexistence of two or three lineages was revealed in about half of the locations on the East European Plain. The most diverse genetic composition of P. notabilis populations was noted in natural forests and slightly disturbed habitats, while the least diverse was in places with a high anthropogenic influence.
28S rDNA, cryptic diversity, genetic lineages, microarthropods, soil fauna, springtails
Parisotoma notabilis Schaeffer, 1896 (Collembola: Isotomidae) is a cosmopolitan species which occurs in almost every biotope in temperate regions of the Western Palearctic, and predominates in most communities of Collembola (
Parisotoma notabilis is morphologically uniform in spite of its occurrence in wide range of habitats (
Genetic variation of P. notabilis suggests lineages may be parapatric as distributional data show some geographical specificity of lineages. Specifically, L1 and L2 are the most widely distributed lineages in Europe; the lineage L1 is widespread in the south and east of Europe, while L2 is found in western and northern Europe and in the Pyrenees. The L0 shows a fairly continuous range from the English Channel and along the coasts of the North and Baltic Seas. The lineage L3 has been found only in Paris and Greece (
In this paper we provide new data on the three lineages of P. notabilis in the eastern regions of Europe and we test two hypotheses: 1) whether the genetic lineages of P. notabilis in the Eastern Europe are distributed parapatrically, as in Western Europe; and 2) whether different genetic lineages of P. notabilis react differently to habitat disturbance.
The study was conducted in the central region of the East European Plain, mainly around Moscow, which includes a wide range of habitats from natural forests to urban lawns. The territory is located in a belt of mixed and broad-leaved forests. The climate is temperate continental, the average annual amplitude of temperature variation is 28 °C, and 600–800 mm of precipitation falls per year (
The extracted material was sorted under a stereomicroscope. The possible mixing with coexisting congeners of P. notabilis was considered. Apart from P. notabilis, four species of the genus Parisotoma have been recorded in the East European Plain: P. agrelli Delamare Deboutteville, 1950, P. ekmani Fjellberg, 1977, P. reducta Rusek, 1984, and P. trichaetosa Martynova, 1977; all four species are rare and only the latter species was recorded in the Moscow region previously. In appearance all four species are easy to separate from P. notabilis by having an almost white corpus and smaller eye spots. The first three congeners occur only in northern areas and are rarely recorded in the central region of the East European Plain. The littoral P. agrelli lives only on the Arctic Ocean shore, while the Asiatic P. reducta is distributed in the very north-east corner the East European Plain. The boreal P. ekmani can probably occur towards the central part of the East European Plain via peat-bogs although it was never recorded there in spite of intensive study of the region (its distribution is given in more detail in
Key differentiating morphological characters of species of Parisotoma recorded in the East European Plain. Abbreviations: Omma: number of ommatidia, Postlab: number of postlabial setae, VT: number of laterodistal setae on ventral tube, Subcx: presence of outer seta on 2-nd subcoxa of first pair of legs, Mucro: number of teeth on mucro, s: number of s-setae on tergites.
Species | Omma | Postlab | VT | Subcx | Mucro | s |
---|---|---|---|---|---|---|
P. notabilis | 3–4 | 4+4 | 3+3 | - | 3 | complete |
P. agrelli | 1 | 3+3 | 3+3 | + | 3 | complete |
P. ekmani | 1 | 4+4 | 4+4 | - | 3 | reduced |
P. reducta | 1 | 3+3 | 3+3 | + | 3 | complete |
P. trichaetosa | 1 | 4+4 | 3+3 | - | 4 | reduced |
The lineages of this species can be identified by both the mitochondrial COI gene and the ribosomal 28S gene (D2 region,
The constructed tree revealed three genetic lineages of P. notabilis: L1, L2, and L4-Hebert (Fig.
Intralineage and interlineage K2P-pairwise distances (%) of the lineages Parisotoma notabilis in the East European Plain for D3–D5 region of 28S gene.
Lineage | Intralineage | Interlineage | ||||
---|---|---|---|---|---|---|
L0 | L1 | L2 | L3 | L4-Saltzwedel | ||
L1 | 0 | 1.23 | 0 | |||
L2 | 0 | 1.23 | 1.41 | 0 | ||
L3 | 0 | 0.70 | 0.89 | 0.53 | 0 | |
L4-Saltzwedel | 0 | 1.59 | 1.77 | 1.06 | 0.88 | 0 |
L4-Hebert | 0 | 0.50 | 0.90 | 1.03 | 0.50 | 1.06 |
Maximum Likelihood genetic tree of six lineages of P. notabilis based on the D3-D5 region of 28S gene fragment (Bootstrap support values shown on the branches, scale bar shows genetic distance) including data from
Numerous cases of sympatry of the lineages were revealed (Fig.
Region | Total number of individuals | Total number of locations | Ratio | Reference |
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Western and Central Europe | 191 | 27 | 0.18* |
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110 | 24 | 0.08 |
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East European Plain | 87 | 21 | 0.5* | This study |
L1 and L4-Hebert lineages were recorded in the urban areas, and all three lineages - in the partly disturbed (forest parks) and undisturbed (forests) habitats. In the forests, the occurrence of L2 and L4-Hebert lineages was about the same, while L1 was sporadic. In forest parks, L1 was the most common, the L4-Hebert was less common, while L2 was rare. In the city (urban areas), L1 absolutely dominated (Fig.
The L1 and L2 lineages of P. notabilis were already cited in the East European Plain (
Previously, studies on the genetic structure of P. notabilis populations showed mainly parapatric distribution of lineages. The simultaneous presence of two or three lineages was noted only in 13% of the total number of locations studied (
Presumably, the number of detected lineages in one location may depend on the number of individuals analyzed from a core. Our data shows, however, that even small samples of 4 or 5 individuals sometimes revealed up to three genetic lineages (Fig.
At present, it is difficult to conclude how widespread sympatry of genetic lineages is. For example, sympatry of genetic lineages was found in Deutonura monticola (Cassagnau) and Heteromurus major (Moniez) among 16 genetically studied Collembola species (
Genetic studies of springtails often do not consider the habitats where the material was collected from, or, at least, do not specify them.
The different habitat preferences of genetic lineages reflect the process of ecological diversification within one species, and can lead to the emergence of new species resulting from ecological speciation. For many taxa, such cases were noted based on the action of different selection vectors according to the gradient speciation model (
Information on the ecological preferences of genetic lineages is sporadic. Thus, in the widespread springtail species Lepidocyrtus lanuginosus the genetic lineage L1 was abundant and occurred in each of the three habitats studied (forests, grassland, arable fields), L2 only in forests, and L3 only in pastures and arable fields (
Our results are preliminary and call for more data. However, the assumption that different genetic lineages of P. notabilis prefer different degrees of habitat disturbance seems convincing at this point. Samples along the disturbance gradient can reveal the diversity of lineages for one location. The cosmopolitan species P. notabilis, abundant in natural and disturbed habitats, is a promising model object for studying the phylogeography of Collembola populations.
Sequencing of the 28S gene is practical and convenient to identify already known genetic lineages while data on the COI gene are needed to describe new lineages. Three genetic lineages of Parisotoma notabilis have been detected in the East European Plain: L1, L2, and L4-Hebert. Mean genetic distances between the lineages in the studied D3–D5 region of ribosomal 28S gene region ranged from 0.9% to 1.4%. About half of the samples in central part of East European Plain included more than one lineage of P. notabilis. The samples from different habitats may include different genetic lineages of the species, which is important to take into account in phylogeographic reconstructions. The most diverse genetic composition of P. notabilis populations was observed in natural forests and forest parks; only two lineages were found in urban environments. Genetic lineages of P. notabilis show ecological specialization: L1 likely prefers disturbed habitats, although L2 and L4-Hebert predominate in natural forests, which requires further research. It is also necessary to focus on the search for characters that could allow the morphological differentiation of the lineages.
The authors are grateful to SE Spiridonov, NV Petrova and MD Antipova for advice on molecular genetic analysis and anonymous reviewers for important comments. This work was supported by Grant No. 22-24-00984 of the Russian Science Foundation.
Sample locations and GenBank Accession numbers of genetic lineages of Parisotoma notabilis.
Habitat | Label | GPS Coordinates | N | Lineage | GenBank Accession number | |
---|---|---|---|---|---|---|
28S | COI | |||||
Urban green | Balash-2021-1* | 55°49'54.1069'N, 37°58'2.7689'E | 1 | L1 | OM714597 | |
ProspVernad-2020-1 | 55°40'54.2149'N, 37°30'22.6072'E | 5 | L1 | OM746101–OM746105 | ||
UgoZapad-2020-1* | 55°39'34.8097'N, 37°28'46.7176'E | 2 | L1 | OM778178, OM778179 | ||
VDNH-2020-1 | 55°48'58.5949'N, 37°39'0.3845'E | 5 | L1 | OM778173–OM778177 | ||
Voronezh-2021-1 | 51°39'33.9962'N, 39°12'7.1375'E | 2 | L1 | OM778153, OM778154, OM778158–OM778160 | ||
3 | L4-Hebert | |||||
Forest Park | Hovrino-2020-1 | 55°52'24.7849'N, 37°28'42.3077'E | 6 | L1 | OM728286–OM728291 | OP861639–OP861643 (L1) |
ProspVernad-2020-2 | 55°41'8.5393'N, 37°30'4.5928'E | 5 | L1 | OM746085–OM746089 | ||
ProspVernad-2020-3 | 55°41'9.5113'N, 37°29'46.7008'E | 3 | L1 | OM746096–OM746098 | ||
ProspVernad-2020-4 | 55°40'53.4301'N, 37°29'59.8372'E | 4 | L1 | OM746081–OM746084, OM746095 | OP866972 (L1) | |
1 | L4-Hebert | |||||
VDNH-2020-2 | 55°48'48.6229'N, 37°39'55.4105'E | 1 | L1 | OM778143, OM778144, OM778150–OM778152, OM778181 | OP861659 (L2) | |
2 | L2 | |||||
3 | L4-Hebert | |||||
Maklino-2021-1 | 54°59'43.8770'N, 36°27'25.7931'E | 5 | L4-Hebert | OM746090–OM746094 | ||
Nature forest | Balash-2020-1* | 55°49'52.4545'N, 37°54'22.9853'E | 1 | L2 | OM714532 | |
OrehZuev-2020-3 | 55°46'43.2060'N, 39°16'13.9757'E | 1 | L2 | OM745895, OM746106–OM746108 | ||
3 | L4-Hebert | |||||
SeloBulat-2021-1* | 55°31'1.9789'N, 37°40'38.7112'E | 2 | L4-Hebert | OM746099, OM746100 | ||
Shakh-2021-1 | 55°56'33.8150'N, 35°31'45.7780'E | 3 | L2 | OM778155–OM778157 | ||
Shakh-2021-2 | 55°55'55.7450'N, 35°37'9.4468'E | 1 | L1 | OM778148, OM778149, OM778169–OM778171 | OP861657 (L2) | |
2 | L2 | |||||
2 | L4-Hebert | |||||
Shakh-2021-3 | 55°56'0.2990'N, 35°37'20.9560'E | 4 | L2 | OM778164–OM778168 | OP861658 (L2) | |
1 | L4-Hebert | |||||
Shakh-2021-5 | 55°59'1.6022'N, 35°35'41.5816'E | 3 | L2 | OM778145–OM778147, OM778180 | ||
1 | L4-Hebert | |||||
Shakh-2021-6 | 55°59'2.4266'N, 35°35'50.4664'E | 2 | L2 | OM757828–OM757831, OM778140, OM778141 | OP861662–OP861664 | |
4 | L4-Hebert | (L4-Hebert) | ||||
Shakh-2021-8 | 55°59'30.6829'N, 36°14'57.8500'E | 1 | L2 | OM778142, OM778161–OM778163 | ||
3 | L4-Hebert | |||||
Shakh-2021-9 | 55°59'14.9005'N, 37°2'57.3605'E | 5 | L4-Hebert | OM778135–OM778139 |