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Article

Resettlement of Eurytemora velox (Crustacea: Copepoda) in Europe, the Urals and Western Siberia

by
Natalia Sukhikh
1,2,*,
Petr Garibian
2 and
Elena Chertoprud
2
1
Zoological Institute RAS, 1 Universitetskaya Embankment, Saint-Petersburg 199034, Russia
2
A.N. Severtsov Institute of Ecology and Evolution, Leninsky Prospect 33, Moscow 119071, Russia
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(1), 47; https://doi.org/10.3390/d16010047
Submission received: 2 November 2023 / Revised: 19 December 2023 / Accepted: 30 December 2023 / Published: 11 January 2024
(This article belongs to the Special Issue Diversity and Biogeography of Microcrustaceans in Continental Waters)
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Abstract

:
The recent distribution of the Ponto-Caspian calanoid copepod, Eurytemora velox, in Western and Eastern Europe has been well-documented; however, there are no studies on the genetic diversity of the recently discovered Western Siberian species population. To contribute towards filling this gap, genetic diversity and distribution were investigated for E. velox collected in the Urals and Western Siberia of the Russian Federation to compare with the European populations. In this study, 44 specimens were dissected for the morphological studies, and 22 specimens of E. velox from different geographical points were analyzed for mitochondrial cytochrome oxidase I (CO1), nuclear ITS1-ITS2 (nITS) and nuclear ribosomal RNA (18SrRNA) gene fragments. Analysis of the CO1 gene region showed that the studied populations from the Urals and Western Siberia differ significantly from European ones and represent a separate genetic line. However, the nuclear nITS and 18SrRNA genes, as well as the results of morphological analysis, did not show such isolation of the Trans-Ural populations from those in Europe. As in many studies on E. velox, we found atypical structural features of the fifth prosomal leg among females in the Ob Bay. Their share was 36% of the number of studied individuals. The CO1 shows that the divergence of genetic lines occurred approximately in the Middle Pleistocene, and the species itself is Paleogene–Neogene by origin. Based on these data, a different scenario of E. velox distribution or possible refuge survival is discussed.

1. Introduction

The significant range extension of Ponto-Caspian Eurytemora velox (Lilljeborg, 1853) in fresh and brackish European waters over the past decades was facilitated mainly due to the distribution of the species, it is supposed, through the big river basins interconnected by human-made canals, so-called migration corridors. The species was described for the first time in 1853 from the Baltic Scania [1] and then recorded in the lagoons of the Northern Caspian–Volga mouth in 1897 [2]. The range of this species covers the area from the Ponto-Caspian and Mediterranean region to Scandinavia, Iceland and the Volga River in Russia [3,4,5,6,7,8,9]. Such a wide range of an admittedly Ponto-Caspian [8] species is supposed to be a result of high species invasiveness.
In 2015–2019, E. velox was found in water bodies of Western Siberia for the first time [10,11,12], particularly in the Yamal Peninsula, as well as in the lower Ob River and its tributaries (below the city of Nizhnevartovsk) in the Ob and Gydan Bays. According to Gerasimova and coauthors [13], the species was also found much further south, in the Irtysh River of the Tyumen region. It is worth noting that intensive hydrobiological studies of the zooplankton in the lower Ob in 1979–2008 [14] resulted in a list of zooplankton species with more than 200 species, but E. velox was not observed at that time. As for Central Siberia, like the Novosibirsk region and further east, the species has not been seen so far [15,16]. In particular, E. velox is not found in the zooplankton of the Lena Delta [17,18,19], although the region has been quite well sampled and studied in recent years due to many ecological programs in the location of the Lena Delta Nature Reserve.
Records of E. velox in the region of the Urals are not documented in the literature sources. All the studies indicate the absence of any eurytemorid copepods in the zooplankton for this region [20,21,22]. The records of the species that are most geographically close to the Urals indicate the presence of E. velox populations in the lower tributaries of the Ural River back to 1923, as found by Muraveysky [23] and, in 1938, by Bening [24]. Repeatedly, in the 1960s, this species was also on the list of zooplankton taxa for that area [25]. In studies of zooplankton in the lower tributaries of the Ural River in 2016 [26], E. velox was not found; the authors noticed that the number of zooplankton taxa has decreased significantly compared to previous observations, and E. velox could not be caught simply with a net. Meanwhile, further south, Kazakh researchers noted the presence of E. velox in small brackish lakes of West Kazakhstan [27,28,29].
No genetic studies have been conducted for the recently found Siberian populations but, considering that E. velox was not there before 2015, it was supposed to be a European invasion [10,11,12].
Genetic studies of E. velox populations from Ukraine, Poland, Belarus and Central Russia (middle Volga River) show the close relationship between those populations [30,31]. Just a few nucleotide substitutions (0.8%) in the CO1 part of the gene differ between the Ukrainian (Black Sea drainage basin) and Central Russian (Caspian Sea drainage basin) populations. The Polish and Belarusian populations are genetically close to that of Central Russia. Here, we present the first study that combines genetic and morphological analysis of the Southern Ural and Ob Bay (Western Siberia) populations of E. velox in comparison with those from Ukraine, Belarus and the Volga reservoirs. Our data offers an interesting insight into the origin of the species and possible ways of spreading in the Urals and Western Siberia.

2. Material and Methods

2.1. Material and Methods Used for Morphological Analysis

Specimens of E. velox from the Rybinsk, Cheboksary and Kuybyshev Reservoirs (Russian Federation), the Feofania ponds in Kyiv (Ukraine) and the Mukhavets River (Belarus) were used for morphological studies (Figure 1, Table 1).
The specimens were identified by the morphological traits identified in [10,34,35].
The samples were sorted under stereomicroscopes (Micromed MC3 Zoom LED (Micromed, Saint Petersburg, Russia) and Olympus SZX10 (Olympus Corp., Tokyo, Japan) and measured with a ToupCam 14.0 MP camera (Hangzhou ToupTek Photonics Co., Hangzhou, China) with the software packages TopView and LevenhukLite (Public joint stock company Levenhuk, Saint Petersburg, Russia). The dissected appendages were placed on slides in pure glycerol, covered with Canadian balsam and a glass cover, and examined at up to 1000× resolution with immersion oil under compound microscopes Olympus CX 22 LED (Olympus Corp., Tokyo, Japan), Levenhuk D870T (Public joint stock company Levenhuk, Saint Petersburg, Russia) and Zeiss IMAGER (Zeiss, Oberkochen, Germany), equipped with the Nomarski system for differential interference contrast microscopy. Photographs were taken under a LOMO BLM-L microscope (LOMO, Saint Petersburg, Russia) equipped with a ToupCam 14.0 MP camera and TopView software version 9.12.226. The final photos were made by combining 8–12 images at different focal depths using the TopView software.
To compare E. velox populations, both sexes were analyzed. In total, 19 different measurements were made (Table 2) based on features proposed in [36]. They are the body size and width, caudal rami length and width, length of the abdominal segments and the number of spines on the exopod of the fifth pair of legs (P5) in the females. For the males, we measured body size, caudal rami length and width, the presence of spines on 10–11 segments of the right antennule and the length proportions of the segments of the P5.
The principal component analysis (PCA) with an unconstrained ordination method was used to test the morphological differentiation between the studied populations in the PAST 4.03 software.

2.2. Genetic Studies

ExtractDNA Blood (Eurogen, RF) was used for lysis, DNA extraction and purification following the manufacturer’s protocol. Species morphological identification was made following the taxonomical keys [8,36].
We obtained sequences of the mitochondrial cytochrome oxidase 1 gene (CO1) and nuclear genes ITS1-ITS2 (nITS) and 18SrRNA. The primers used for the amplifications were cited in the article by Sukhikh and coauthors [35]. The used conditions of the CO1 PCR are published in our previous work [35]. The PCR conditions for the used sets of primers started with DNA denaturing at 95 °C for 30 s, followed by 38 cycles of 30 s denaturing at 95 °C, 30 s, annealing at 50 °C for the nITS and 55 °C for the 18SrRNA, 70 s of extension at 72 °C and then a final extension at 72 °C for 7 min.
The amplification products were purified with a Cleanup Mini purification kit (Eurogen, RF), then sequenced using a 3500xL Genetic Analyzer with a BigDye Terminator v3.1 Cycle Sequencing Kit. Both DNA strands were sequenced to confirm the accuracy of each sequence.
The sequences were aligned using the algorithm CLUSTAL W [37] implemented in BIOEDIT v.7.2 [38], with manual editing of ambiguous sites.
Phylogenetic reconstructions were performed by maximum likelihood (ML) and a general time–reversible model with gamma rate distribution (G), and without invariable sites (I), with the MEGA XI software package [39]. The best-fitting model under the ML criterion was selected from the “Bayesian Information Criterion” (BIC) and “Akaike Information Criterion” (AIC) output of jMODELTEST v0.1.1 [40]. The level of nucleotide differences between the species was calculated with the Tamura–Nei 93 model, as commonly used for Eurytemora species [31,32,34,35,41], in the MEGA XI software package [39].
Paleontological information and points based on molecular phylogenetic data were used for the estimation of possible divergence age for different clades. The maximum likelihood test in MEGA XI was applied to test the fit of our data to molecular clock models [39,42]. Nucleotide substitution parameters (using a maximum likelihood substitution model statistical method) were also made in MEGA XI, based on the lowest BIC (Bayesian information criterion) scores. The null hypothesis of equal evolutionary rate throughout the tree was not rejected at a 5% significance level.
The divergence times of lineages were estimated using BEAST2 (ver. 2.6) [43] with Bayesian inference, using the calibrated Yule model for the tree prior and the strict clock model. BEAST2 used a random tree with 6 × 106 generations and a sample frequency of 5 × 103 generations. We chose the rate of substitutions of 2.8% per MYR, as no properly calibrated rate estimates are available for copepods, in particular, and for other crustaceans, estimates of COI rates in the range of 1.4% to 4% divergence per MYR have been obtained [44,45,46,47,48]. The chosen value yields results that are congruent with the paleontological data.
As calibration points of the species and genetic lineages (with 15% standard deviations), the fossil-based minimum age was applied for the split: Lepidurus/Triops 122 MYA [49,50], plus, additional calibration points based on molecular phylogenetic data were used within the outgroups: Acartia–Eurytemora—170 MYA [51], Acanthocyclops–Mesocyclops group—24 MYA [51] and inner group Eurytemora aff. affinis–Eurytemora carolleeae—11.5 MYA [41].

3. Results

3.1. Genetic Studies

Sequences of the mitochondrial cytochrome C oxidase 1 gene (CO1) and nuclear genes ITS1–ITS2 (nITS) and 18SrRNA from E. velox specimens collected in the Ob Bay and a lake in Magnitogorsk were obtained (Table 3). All the other sequences for the rest of the populations were used from published data [31,32,52] for comparison (Table 3).
The results of the CO1 (520 bp length) gene region analysis showed that the specimen from the Ob Bay is identical to the E. velox population from Chelyabinsk and belongs to one shared haplotype (Figure 2). These populations in the CO1 gene differ from the previously studied E. velox from Europe [36] by 4%.
The results of the nITS (803 bp length) gene region analysis showed that three specimens from the Ob Bay and Magnitogorsk are represented by three different haplotypes, one of which is shared with one of the Chelyabinsk haplotypes (Figure 2). These haplotypes are closer to the Volga population [31], which differs from the Kyiv one by 0.1% of nucleotide substitutions.
Analysis of the DNA sequences of the conservative 18SrRNA (333 bp length) gene showed no differences among the studied populations of E. velox from the Ob Bay, Chelyabinsk, Kyiv and the Volga, as expected.
Our molecular clocks revealed a Paleogene–Early Neogene E. velox origin (13.3–41.1 MYA). The European and the Ural–Siberian lineages of E. velox were differentiated possibly in the mid-Pleistocene 0.133–0.928 MYA according to our molecular clock calibration (Figure 3).

3.2. Morphological Studies

Among all of the studied populations, the population from Ob Bay turned out to be the most variable in the morphology of the P5 in females and the biggest in body size for both males and females. In this population, Exp I of the P5 in females was found to be morphologically highly variable (Figure 4, Table 2).
The proportion of females with a P5 structure deviating from the normal with one spine on exopod 1 was very high (four out of eleven individuals)—36% in the Ob Bay population. In the Belarusian specimens, one of the six studied females had two spines on one of the exopods on the P5. Among the other studied populations, we did not observe deviations from the normal morphology, and all the P5s of females had a standard structure with one spine on exopod 1. All males of the population from Magnitogorsk and Ob Bay had spines on the 10th and 11th segments of the geniculate antennae (Figure 5). In the Belarusian population, among the four studied males, we observed either the absence or presence of these spines. No spines at all on the 10–11 segments of the geniculate antennae of males were observed on specimens from the Rybinsk Reservoir.
To assess the morphological variability between the studied populations of females, the following indices were calculated: L/W Body, Furcal L/W, Furcal W/Body W, Furcal W/Body L and abdominal segment length ratio indices 1–3 (Table 2). The indices used among females showed that, as in the genetic data, the Belarusian and Volga populations do not differ significantly from each other. The populations of Belarus and Ukraine differ in one index (L/W Body). At the same time, the populations from Magnitogorsk and Ob Bay differ significantly from each other, both in body size and in the proportions of furcal branches and abdominal segments, as well as in the degree of variability of the P5. Females from the Ob Bay population are larger in size, have thinner and longer furcal rami, and the first segment of the abdomen is longer than in individuals from the population of reservoirs near Magnitogorsk (Table 2, Figure 5A and Figure 6A).
These populations also differ in the following indices: L/W Body, Furcal L/W, Furcal W/Body W, Furcal W/Body L and L abdominal segment 1/L abdominal segment 2. As for the general appearance of females from all the studied populations—the ones from Kyiv have the slimmest shape and the highest L/W Body index (3.9 +/− 0.06). They are also the largest of all: the body length is 1.85 +/− 0.11 mm. The stockiest females came from the Ob Bay; their L/W Body ratio is 2.89. The population from the Rybinsk Reservoir had the smallest size of all the females studied—1.43 +/− 0.06 mm. The longest furcae in comparison with their width were found in females from Kyiv—almost seven times longer than the width. The average for the population from Kyiv was 5.83 +/− 0.18. Slightly shorter furcae were observed in females from the Ob Bay—5.73 +/− 0.05. The next population in terms of the length/width ratio of furcae is the Belarusian one—5.27 +/− 0.15. In the Volga population from the Rybinsk Reservoir and the population of females from the Urals; the ratio was 4.67 +/− 0.2 and 5.06 +/− 0.07, correspondingly. The Ob Bay and Ural populations of females have the shortest furcae in relation to the length of the entire body; the index fluctuates in the range of 6.79–9.53. In European populations, this index is approximately the same on average and does not exceed 7.77.
On a PCA plot built using the indices, females look more or less uniform. The PCA showed the maximum weight of furcal index and body length/width ratio (Figure 7A).
To assess the morphological variability between the studied populations of males, the ratio indices of the segments of the left and right parts of the P5, as well as Furcal L/W, Body L/Furcal L, Furcal W/Body W, Furcal W/Body L, were measured (Table 2). Among the males, the Belarusian and Volga populations also do not significantly differ from each other in any of the selected indices. At the same time, genetically identical populations from Magnitogorsk and Ob Bay differ significantly from each other in body size, proportions of furcal rami and P5 segment lengths. Specimens from the Ob Bay population have larger sizes, thinner and longer furcal rami, as well as shorter bases of the left P5 and the first exopod segment of the right leg P5 relative to the coxa than in individuals from the population of reservoirs near Magnitogorsk. (Figure 5B and Figure 6B). Populations from the Ob Bay and Magnitogorsk have significant differences in the following indices: Furcal L/W, Body L/Furcal L, Furcal W/Body W, Left P5 Bas/Cox and Right P5 Exo1/Cox (Table 2). The Ob Bay and Magnitogorsk populations are significantly different from the Volga and Belarusian populations according to all the selected Left P5 indices. The Magnitogorsk and Belarusian populations also differ in the ratio of the lengths of exopods 1–3 to the length of the Right P5 coxa (Exo/Cox). The Belarusian population differs from the Ob Bay population in the ratio of the lengths of the basipod, exopod 3 and coxa (Bas/Cox, Exo3/Cox). The largest males were found in the Ob Bay (1.69 +/− 0.11 mm) and the smallest in Belarus (1.09 +/− 0.17 mm). The longest furcae in comparison with the width were observed in males from the Ob Bay; the length/width ratio is 7.24 +/− 0.07, and the shortest are in males from the Rybinsk Reservoir (Volga region); the index does not exceed six.
On the PCA plot, built using the indices, Ob Bay males appear the most isolated. The PCA showed the maximum weight of furcal index and the ratio of furcal length to whole body length (Figure 7B).

4. Discussion

4.1. Morphological Studies

According to a study by Gaviria and Forro [36], almost all the populations they studied from Austria, Hungary and Romania, belonging to the Black Sea basin, had variability in the structure of the P5 of females and had spines on the 10–11 segments of the male geniculate antennae. Variation in the structure of the P5 of females was also noted for other European populations (Poland, France and Hungary) [52,53,54]. It is supposed that such variability is connected with environmental stress as a result of human activity (pollution, hydraulic work, etc.) [36]. There is also a hypothesis that this is a result of species hybridization between E. velox and E. affinis [32,55], although these species are never found cohabiting. In our studies, among populations of E. velox from the basins of four seas, the Caspian, Black, Baltic and Kara Seas, populations from the Ob Bay and Belarus show the highest variability in terms of the mentioned above morphological characteristics, while other populations (Volga region, Kyiv) have stable structural features typical of E. velox. But in general, we did not find significant morphological differences among all the studied populations.

4.2. Genetic Studies

The results of the CO1 and nITS gene region analysis showed that the specimens from the Ob Bay are close to the E. velox population from Chelyabinsk, which was studied earlier [32]. The Southern Ural populations (Chelyabinsk and Magnitogorsk) differ in the CO1 gene from the previously studied E. velox from Europe [31] by 4% (Figure 2A), which corresponds to the subspecies level among Copepoda [35,56,57]. Interestingly, the nITS genes did not show such homogeneity of the populations from the Southern Urals, and eight sequences are represented by five haplotypes that differ from each other by 1–2 replacements (Figure 2B). These haplotypes are identical to the Kyiv and Volga populations [31], which differ by 0.1% of nucleotide substitutions in the nITS genes.
Analysis of the DNA sequences of the conservative 18SrRNA gene shows no differences between the studied populations from the Ob Bay, Chelyabinsk (Southern Urals), Kyiv, and the Volga of E. velox, as expected. A similar picture, when we observe high intraspecies and species divergence in mitochondrial genes and very low one among nuclear genes, was observed among different groups of Copepoda [35,56,57]. It was shown that the level of interspecific differences in the CO1 gene among Eurytemora is 12.0–30.2%. The nuclear 18SrRNA gene is more useful in a wide phylogenetic analysis, and the level of pairwise divergence among the Eurytemora species is 0.4–12.9%. The level of differences among Eurytemora species in nITS genes is 4.9–34.5%.
Data from molecular clock calculations based on a region of the mitochondrial CO1 gene showed that E. velox appeared approximately at the end of the Paleogene–early Neogene (13.3–41.1 MYA). The divergence within the species into European (Ponto-Caspian) and Ural-Siberian lines occurred no later than 0.928 MYA, which is approximately in the Middle Pleistocene, probably during one of the interglacial phases. Later, the Ponto-Caspian E. velox split into the Volga and Black Sea genetic lines. We assume that the common ancestor of all present populations survived glaciation in a refuge in the Ponto-Caspian region. From there, judging by the network of CO1 haplotypes, one lineage spread towards Europe and later split up into two other lineages (probably the Black Sea and Caspian), while the other line spread along the eastern part of the Ural Mountains and gave source to the Ural–Siberian populations. The common origin of all the lines is confirmed by the structure of the haplotype network, built on sections of nuclear genes, nITS, in which we see that some of the Ural haplotypes are grouped with the Ukrainian and some with the Cheboksary haplotypes.

4.3. Urals and Western Siberian Populations

Considering the significant number of previous studies on the zooplankton species composition in the reservoirs of Chelyabinsk and Magnitogorsk [20,21,22], the recent appearance of E. velox obviously indicates an invasive nature. Until recently, long-term studies of the lower reaches of the Ob Bay (1979–2008) also did not reveal the presence of this species [14], although there is no data on this species for the Ob Bay. Taking into account the proximity of the studied reservoirs to the lower Ural River, where the population of E. velox has long been known [23,24], it is possible that this population is a donor for the Chelyabinsk region and the Arctic coast of the Western Siberia. At the same time, despite the short distance between Magnitogorsk and Chelyabinsk, which is only three hundred kilometers, Magnitogorsk stands on the Ural River, which flows into the Caspian Sea, and the reservoirs of Chelyabinsk already belong to the Kara Sea basin, as does the Ob Bay. Considering the migration routes of birds, a bird-mediated dispersal ability by diapausing eggs [56,57] may explain the existence of these two populations divided by a geographical barrier, although, for species of the genus Eurytemora, there is no confirmed evidence of this fact in the literature. The most common means of the genus invasion is in the ballast water of ships. Hovewer this seems unlikely since the drainage basins of the Caspian and Kara Seas are not connected. We can assume that the species spread in Siberia naturally along water corridors from the lower Ural River to the Arctic coast. Nevertheless, given the huge distance covered and the geographical barrier—a watershed between the basins of the Caspian and Kara Seas, this hypothesis needs more confirmations. The origin of the Trans-Ural population of E. velox from the Caspian Sea and spread in the Ural River seems to us the most likely. Unfortunately, we do not have for study genetic material from the lower Ural River, the basin of the Caspian Sea. Furthermore, the data from another population inhabiting the northern tributary of the Caspian Sea—the Volga River and its drainage basin—do not confirm this hypothesis, since the Volga populations show genetic similarity to the European ones, but not to the Trans-Ural populations [31]. It is obviously that the increase in sampling efforts in the Caspian region and Siberia is needed and future genetic studies will help to identify pathway of distribution. In general, a similar pattern of different genetic lineage distribution within one drainage basin and within small areas is also known for other species of the genus Eurytemora [35].
Due to the lack of studies on the Ob Bay before the recent data, it should not be excluded that the bay mouths in Western Siberia (Ob Bay, Gydan Bay) are the natural habitats for this species. Those areas might be the initial spot from where E. velox began to spread toward the south and explains E. velox records in the lower Ob River up to Nizhnevartovsk only in recent years [11] and our new records of species in Chelyabinsk and Magnitogorsk. In this case, the idea of a reverse direction in the Siberian invasion of E. velox from the north to the southern Ponto-Caspian reservoirs may explain such a pattern in genetic results. In addition, it cannot be excluded that we are observing in Siberia not an invasive species, but a species having a disrupted range as a result of the last glaciation.
Another possible scenario for the appearance of E. velox populations under study in the Urals and Western Siberia is the introduction of populations from Europe that we have not yet studied, at least genetically. For example, in the article by Gaviria and Forro [36], several populations from the Black Sea drainage basin (Danube River from Austria to Romania) are morphologically described, and, according to the available data, these several studied populations themselves look quite heterogeneous in a small area. Nevertheless, we do not see any significant differences between our specimens and those described in this article. In general, according to the morphological indices and appearance of females from Regelsbrunn (Austria), cited in the article by Gaviria and Forro [36], this Austrian population looks most similar to the Volga eurytemoras. Also, the population from the Baltic region has not been genetically studied, except for the findings about the invaders in Belarus and Poland, genetically identical to the Volga population [30,31]. The morphological works of Kiefer [58] and Lucks [52] describe Eurytemora from water bodies of Germany and Poland (again the Baltic region) showing variability in relation to the P5 in females, although spines on the 10–11 segments of the geniculate antennae were invariably present.

4.4. Baltic Population

In addition to populations from Belarus, Poland and Germany, fresh and brackish water populations from the Neva River, the Gulfs of Finland and Bothnia are also known from the Baltic region [2]. Probably, unlike the Belarusian and Polish populations of invaders, these populations are native. Unfortunately, we were unable to find any of these populations, despite annual sampling in the Neva River and in the Gulf of Finland. Material from the Gulf of Bothnia was also available to the author, but it did not contain the species sought. It was assumed that, in addition to the Ponto-Caspian refuge, the species could survive glaciation in a certain Baltic refuge (Littorina Sea), from which the Baltic population originated [59]. It seems that today, if these ancestral populations exist, they inhabit very limited habitats.
It should be noted that the original description of the species E. velox was made specifically of those from the Baltic Sea—the coast of the Gulf of Bothnia in Sweden [1]. In the picture of the male in the original description, we see extremely narrow and long furcal rami, the length/width ratio of which is 12, and the ratio of body length to furcal length is 5.52. We did not observe such values for any of the populations we studied or previously described. At the same time, the female furcal index of 5.3–5.5 is quite consistent with our data, although the ratio of abdominal segments differs: 1.38/1/1.83. It is also worth noting that the original description does not provide information about the variability of the P5 structure in females. In general, this population could be special and different from the populations we studied in Europe and could be the possible progenitor of the Trans-Ural E. velox.
Thus, we observed a new CO1 genetic lineage of E. velox from the Trans-Ural region, which does not differ in the nITS and 18SrRNA part of genes from known ones from Europe. The origin of the E. velox species in the Urals and Western Siberia remains not entirely clear. It is obvious that the species is currently actively spreading beyond the Urals and Western Siberia. We can say with certainty that the source, in this case, is not the populations we studied from Europe since, genetically, the European populations are significantly different and diverged from the Trans-Ural populations about the Middle Pleistocene according to our date.

Author Contributions

N.S. and E.C.: conceptualization of the paper; N.S. and E.C. wrote the main manuscript text and prepared the figures; validation, P.G. All the authors discussed the results and commented on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The studies were supported by the Russian Science Foundation, 22-14-00258.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author. Accession numbers for sequences provided in Table 3 can be found in GenBank (https://www.ncbi.nlm.nih.gov accessed on 12 December 2023).

Acknowledgments

We are very grateful to Larysa Samchyshyna IF NAAS for the valuable comments and great im-proving of the paper. We are thankful to Valentina Lazareva, IBIV RAS, Vasilii Vezhnovets, NAS of Belarus, Alisa Neplyukhina, IEE RAS and Maria Baturina IB, Komi SC UB RAS for their help in sampling. We also thank the anonymous reviewers and editor-in-chief for their careful reading of our manuscript and their many insightful comments and suggestions. The genetic part of the work was performed in the Core Facilities Centre “Taxon”, ZIN RAS, and sequencing was performed in the Evrogen Joint Stock Company (Moscow).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of studied populations of Eurytemora velox: 1—Rybinsk Reservoir; 2—Cheboksary Reservoir; 3—Kuybyshev Reservoir; 4—Zavodskoy Pond on the Ural River in Magnitogorsk (Chelyabinsk Region); 5—Smolino Lake in Chelyabinsk (Chelyabinsk Region); 6—Ob Bay (Yamal Region); 7—Mukhavets River (Brest region); 8—Feofania ponds (Kyiv).
Figure 1. Map of studied populations of Eurytemora velox: 1—Rybinsk Reservoir; 2—Cheboksary Reservoir; 3—Kuybyshev Reservoir; 4—Zavodskoy Pond on the Ural River in Magnitogorsk (Chelyabinsk Region); 5—Smolino Lake in Chelyabinsk (Chelyabinsk Region); 6—Ob Bay (Yamal Region); 7—Mukhavets River (Brest region); 8—Feofania ponds (Kyiv).
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Figure 2. Median-joining network of haplotypes of Eurytemora velox built on 11 and 19 nucleotide sequences of the CO1 (A) and nITS (B) part of genes. The lines indicate the number of mutations between haplotypes. Circles are proportional to the haplotype frequency.
Figure 2. Median-joining network of haplotypes of Eurytemora velox built on 11 and 19 nucleotide sequences of the CO1 (A) and nITS (B) part of genes. The lines indicate the number of mutations between haplotypes. Circles are proportional to the haplotype frequency.
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Figure 3. Phylogenetic ultrametric tree constructed in BEAST2 v.2.6 for Eurytemora velox. Phylogenetic analysis of the mitochondrial data set (CO1) with strict clock estimates based on fossil calibration point (Lepidurus/Triops 122 MYA). Statistic support (posterior probabilities (BI)) of branches is coded by the color gradient from pink (low) to blue (high). Probable time of divergence between clades (in MYA) based on the rate of substitutions of 2.8% per MYA given in nodes.
Figure 3. Phylogenetic ultrametric tree constructed in BEAST2 v.2.6 for Eurytemora velox. Phylogenetic analysis of the mitochondrial data set (CO1) with strict clock estimates based on fossil calibration point (Lepidurus/Triops 122 MYA). Statistic support (posterior probabilities (BI)) of branches is coded by the color gradient from pink (low) to blue (high). Probable time of divergence between clades (in MYA) based on the rate of substitutions of 2.8% per MYA given in nodes.
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Figure 4. Females of Eurytemora velox from the Ob Bay (Yamal Region): (A–D)—different types of leg 5. Scale 50 µm—(A–D).
Figure 4. Females of Eurytemora velox from the Ob Bay (Yamal Region): (A–D)—different types of leg 5. Scale 50 µm—(A–D).
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Figure 5. Eurytemora velox from the Ob Bay (Yamal Region): (A)—female: (B)—male; (C)—leg 5 of male; (D)—7–14 segments of male antennule (ventral). Scale 500 µm—(A,B); scale 50 µm—(C); scale 30 µm—(D).
Figure 5. Eurytemora velox from the Ob Bay (Yamal Region): (A)—female: (B)—male; (C)—leg 5 of male; (D)—7–14 segments of male antennule (ventral). Scale 500 µm—(A,B); scale 50 µm—(C); scale 30 µm—(D).
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Figure 6. Eurytemora velox from the Zavodskoy Pond in Magnitogorsk (Chelyabinsk Region): (A)—female; (B)—male; (C)—P5 of female; (D)—P5 of male. Scale 500 µm—(A,B); scale 50 µm—(C,D).
Figure 6. Eurytemora velox from the Zavodskoy Pond in Magnitogorsk (Chelyabinsk Region): (A)—female; (B)—male; (C)—P5 of female; (D)—P5 of male. Scale 500 µm—(A,B); scale 50 µm—(C,D).
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Figure 7. Two-dimensional PCA ordination of Eurytemora velox female (A) and male (B) populations on the two first axes. Morphological indices are indicated as vectors.
Figure 7. Two-dimensional PCA ordination of Eurytemora velox female (A) and male (B) populations on the two first axes. Morphological indices are indicated as vectors.
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Table 1. Studied material of Eurytemora velox.
Table 1. Studied material of Eurytemora velox.
Sampling SiteDrainage BasinNumber of Morphologically Studied SpecimensNumber of Genetically Studied SpecimensDate of SamplingCollector
Rybinsk Reservoir, RussiaVolga River, Caspian Sea basin8 females 2017Valentina Lazareva, IBIV RAS
Cheboksary Reservoir, RussiaVolga River, Caspian Sea basin1 female4 females2020Valentina Lazareva, IBIV RAS [31]
Kuybyshev Reservoir, RussiaVolga River, Caspian Sea basin1 female 2018Valentina Lazareva, IBIV RAS
Feofania ponds, UkraineDnieper River, Black Sea basin7 females3 females2020Larysa Samchyshyna, IF NAAS [31]
Mukhavets River, BelarusWestern Bug, Baltic Sea basin6 females 2019Vasilii Vezhnovets, NAS of Belarus
Ob Bay, RussiaKara Sea basin11 females2 females2022Petr Garibian,
IEE RAS
Magnitogorsk LakeOb River, Kara Sea basin14 females2 females2022Alisa Neplyukhina, IEE RAS
Lake Smolino, Southern Urals region, RussiaOb River, Kara Sea basin 7 females2021Maria Baturina, IB Komi SC UB RAS
[32]
Dziwna Channel, PolandBaltic Sea basin 4 specimens2020[33]
Table 2. Measurements and morphometric indexes in studied populations of Eurytemora velox. Mean ± standard deviation (Min–Max), +/− is presence or absence.
Table 2. Measurements and morphometric indexes in studied populations of Eurytemora velox. Mean ± standard deviation (Min–Max), +/− is presence or absence.
TraitGulf of ObMagnitogorskKyivBelarusRybinsk ReservoirCheboksary ReservoirKuibyshev Reservoir
Female
Body length, mm mean +/− SD1.85 +/− 0.111.61 +/− 0.061.77 +/− 0.021.51 +/− 0.021.43 +/− 0.061.481.52
Body length, mm range1.63–1.971.54–1.721.68–1.861.42–1.581.68–1.87
N of studied individuals111476811
Body Length/Weight 2.893.163.9 +/− 0.063.5 +/− 0.083.6 +/− 0.093.323.31
Thoracic wings+++++++
Abdominal segments 1–3 length ratio1.62/1/1.831.53/1/1.841.71/1/1.971.79/1/1.871.68/1/1.931.79/1/1.821.88/1/1.8
Furcal L/W5.73 +/− 0.055.06 +/− 0.075.83 +/− 0.185.27 +/− 0.154.67 +/− 0.2
Furcal L/W range5.48–5.954.74–5.624.84–6.934.42–6.164.31–6.17
Body L/Furcal L7.91 +/− 0.148.3 +/− 0.205.91 +/− 0.096.28 +/− 0.166.47 +/− 0.08
Body L/Furcal L range6.79–8.486.91–9.535.37–6.585.57–7.776.16–6.91
Furcal W/Body W0.06 +/− 0.000.08 +/− 0.000.12 +/− 0.000.11 +/− 0.000.12 +/− 0.00
Furcal W/Body W range0.06–0.070.06–0.090.10–0.140.10–0.130.10–0.13
Furcal L/Body W0.37 +/− 0.010.39 +/− 0.010.69 +/− 0.150.58 +/− 0.020.58 +/− 0.15
Furcal L/Body W range0.34–0.40.35–0.460.58–0.780.46–0.640.52–0.65
Furcal W/Body L0.02 +/− 0.000.02 +/− 0.000.03 +/− 0.000.03 +/− 0.000.03 +/− 0.00
Furcal W/Body L Range0.021–0.0250.020–0.0280.025–0.0360.028–0.0340.026–0.034
P5th leg. Exo. 1
P5 right leg/left leg: one spine/one spine+++++++
P5 right leg/left leg: one spine/two spines+−−−−−−
P5 right leg/left leg: two spines/one spine+−−+−−−
P5 right leg/left leg: two spines/two spines+−−−−−−
Male
Body length mean +/− SD1.69 +/− 0.111.35 +/− 0.1 1.09 +/− 0.171.14 +/− 0.01
Body length range1.54–1.861.23–1.51 1.06–1.131.12–1.15
N of studied individuals1111 42
Right 1st antennular spine 10++ +/−−
Right 1st antennular spine 11++ +/−−
Furcal L/W7.24 +/− 0.075.92 +/− 0.13 5.86 +/− 0.165.43 +/− 0.46
Furcal L/W range6.88–7.654.85–6.43 5.24–9.465.17–6.04
Body L/Furcal L6.67 +/− 0.277.85 +/− 0.29 6.00 +/− 0.097.54 +/− 0.26
Body L/Furcal L range5.74–8.456.75–9.44 5.64–6.366.86–8.05
Furcal W/Body L0.021 +/− 0.0010.022 +/− 0.001 0.029 +/− 0.0010.025 +/− 0.002
Furcal W/Body L range0.017–0.0240.018–0.026 0.026–0.0320.021–0.028
Left 5th leg length ratio Cox:Bas.:Exo1:Exo21/1.46/1.7/2.251/1.6/1.8/2.2 1/1.15/1.38/1.731/1.2/1.4/1.9
Right 5th leg length ratio Cox:Bas:Exo1:Exo2:Exo31/2.3/2.4/2.16/1.551/2.3/2.8/2.3/1.5 1/2.1/2.3/2.0/1.831/2.0/2.3/1.9/1.7
Table 3. Sequences with accession numbers of GenBank used in the study.
Table 3. Sequences with accession numbers of GenBank used in the study.
Sampling PlaceCO1nITS18SrRNASource
Cheboksary Reservoir, Russia2 sequences MZ373321-MZ3733223 sequences MZ400502-MZ4005041 sequence
MZ373302		[31]
Feofania ponds in Kyiv, Ukraine3 sequences MZ373318-Z3733203 sequences MZ400499-MZ400501OR921659[31]
Gulf of Ob, RF1 sequence
OR578622		1 sequence OR5830342 sequences OR578728-OR578729This paper
Magnitogorsk Lake, Russia 2 sequences OR583032-OR5830332 sequences OR921657-
OR921658		This paper
Lake Smolino, Southern Urals region, Russia3 sequences
OR578619-OR578621		7 sequences OR583025-OR5830313 sequences OR578725-OR578727[32]
Dziwna Channel, Poland2 sequences MT146446-MT1464453 sequences MT787212-MT787214 [33]
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Sukhikh, N.; Garibian, P.; Chertoprud, E. Resettlement of Eurytemora velox (Crustacea: Copepoda) in Europe, the Urals and Western Siberia. Diversity 2024, 16, 47. https://doi.org/10.3390/d16010047

AMA Style

Sukhikh N, Garibian P, Chertoprud E. Resettlement of Eurytemora velox (Crustacea: Copepoda) in Europe, the Urals and Western Siberia. Diversity. 2024; 16(1):47. https://doi.org/10.3390/d16010047

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Sukhikh, Natalia, Petr Garibian, and Elena Chertoprud. 2024. "Resettlement of Eurytemora velox (Crustacea: Copepoda) in Europe, the Urals and Western Siberia" Diversity 16, no. 1: 47. https://doi.org/10.3390/d16010047

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