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Article

Discovery of a New Species of Daphnia (Crustacea: Cladocera) from the Arabian Peninsula Revealed a Southern Origin of a Common Northern Eurasian Species Group

1
Department of Biology, College of Science, United Arab Emirates University, Al Ain, Abu Dhabi P.O. Box 15551, United Arab Emirates
2
A.N. Severtsov Institute of Ecology and Evolution, 119071 Moscow, Russia
3
Khalifa Center for Genetic Engineering and Biotechnology, United Arab Emirates University, Al Ain, Abu Dhabi P.O. Box 15551, United Arab Emirates
4
I.D. Papanin Institute for Biology of Inland Waters, 152742 Borok, Russia
*
Authors to whom correspondence should be addressed.
Water 2022, 14(15), 2350; https://doi.org/10.3390/w14152350
Submission received: 17 June 2022 / Revised: 16 July 2022 / Accepted: 27 July 2022 / Published: 29 July 2022
(This article belongs to the Special Issue Species Richness and Diversity of Aquatic Ecosystems 2.0)

Abstract

:
The biodiversity distribution patterns and their formation history in continental waters are studied based on some model groups such as Daphnia O.F. Müller (Crustacea: Cladocera). Most publications on this genus concern the subgenus Daphnia (Daphnia) while representatives of the subgenus Daphnia (Ctenodaphnia), inhabiting mainly temporary waters, are poorly studied. We found a new species of the D. (C.) sinensis complex in the deserts of the Arabian Peninsula, and our discovery allows us to resolve some problems concerning the history of these daphniids in the northern hemisphere. A formal description, illustrations (including numerous SEM photos) and a differential diagnosis of D. (C.) arabica Neretina, Al Neyadi & Hamza sp. nov. are provided. Phylogeny of D. (C.) similis complex is reconstructed based on three mitochondrial genes (12S, 16S and COI); a haplotype network based on short 12S fragments is also constructed. A monophyletic D. (C.) sinensis within the D. (C.) similis complex includes three earlier-derived locally distributed members: D. (C.) similoides, D. (C.) inopinata and D. (C.) arabica sp. nov. Our data suggest an old (Late Mesozoic) Gondwanan origin of the D. (C.) sinensis group and its Caenozoic differentiation in North Africa and the Middle East. This region then became a center of subsequent dispersion of D. (C.) sinensis through the whole of Eurasia and Africa during the Miocene and subsequent epochs. Interestingly, our scheme of the D. sinensis group dispersion has a well-known analogue: it is comparable to that suggested for earlier human migration from Africa through the Arabian Peninsula and the Middle East to the rest of Eurasia.

1. Introduction

Freshwater biodiversity is studied disproportionately both in taxonomic and geographic aspects. Indeed, some groups, such as fishes [1,2], are well-studied through the world, while the diversity of other animals such as the water fleas (Crustacea: Cladocera) is greatly underestimated [3,4]. Some regions, such as Europe and North America, are well-studied, while for some other regions, we do not even have lists of the usual freshwater taxa [5]. More modern genetic methods, such as genetic barcoding [6,7], contribute to our understanding of qualitative and quantitative aspects of biodiversity distribution, but they cannot replace traditional taxonomy and faunistic studies [8]. Moreover, the results of barcoding sometimes need to be especially decoded due to imperfect identification of the species whose sequences are deposited to Genbank, BOLD and other databases [9,10].
The biodiversity distribution patterns and their evolutionary history in continental waters have been studied based on some cladoceran model groups, such as Daphnia O.F. Müller, which is also a well-known model of ecology and physiology [11,12,13]. Since pioneer phylogeographic studies on the water fleas [14,15,16], several groups of Daphnia became models of phylogeographic studies on regional [17,18,19,20,21] and global [22,23,24,25] scales. Most publications concern the subgenus Daphnia (Daphnia) O.F. Müller, first of all, the D. longispina species group [26,27] inhabiting mainly large water bodies. At the same time, temporary waters of different continents are populated by other daphniids, including numerous representatives of the subgenus, D. (Ctenodaphnia) Dybowski & Grochowski [28,29]. Except for D. (C.) magna Straus, which is a model species in toxicological studies [30,31], these taxa attract little attention from hydrobiologists. A global phylogeographic analysis was conducted for D. (C.) magna only [32,33]. It was found that, in general, D. magna demonstrates a phylogeographic pattern similar to that revealed in other pelagic [34] or neustonic [25] cladocerans.
The idea of geographic domination of former Gondwana regions by the subgenus Daphnia (Ctenodaphnia) Dybowski et Grochowski, 1895 and of former Laurasian regions by the subgenus Daphnia (Daphnia) was popular in the 20th century [22,35]. However, this point of view was based on fossil records of both Daphnia (Daphnia) and Daphnia (Ctenodaphnia) ephippia from the Jurassic/Cretaceous boundary [36]. New evidence of a very old speciation of major clades was obtained recently [37]. However, large-scale transcontinental studies are very rare for Daphnia [23] and some regions of the planet are still poorly studied.
Few ctenodaphniid taxa are known from within the whole of Eurasia, although this is the largest continent in the planet. Moreover, most taxa of the subgenus are known from within the Mediterranean region [38], while only three species complexes are distributed in more northern regions: D. similis, D. atkinsoni and D. magna complexes, with few species in each [22,39,40]. It was shown that the similis-like Daphnia in the Holarctic are represented in reality by two different branches: D. similis complex in Eurasia and D. exilis complex in the Americas [22]. Popova et al. [40] have revised the former and found four different species: D. similis Claus, 1876; D. sinensis Gu, Xu, Li, Dumont et Han, 2013; D. similoides Hudec, 1991 and D. inopinata Popova et al., 2016.
However, we found a new species from this complex in the deserts of the Arabian Peninsula (specifically in the eastern region of the United Arab Emirates), and our discovery allows us to resolve some problems concerning the history of these daphniids in the northern hemisphere based on its mitochondrial phylogeny.

2. Materials and Methods

2.1. Sampling and Morphological Analysis

In mid-March 2018, we collected a sediment core in a dry basin on the upstream side of Al Shuwaib dam (see the map in [41]). The sediments were poured into a 2 L beaker and covered with desalinated bottled commercial drinking water at room temperature (20 ± 1 °C), under 12:12 h light/dark conditions for about 2 weeks. At the beginning of the third week, a few drops of freshly harvested unicellular monoclonal culture of Chlorella vulgaris were added to the surface water covering the sediments. A few days after the addition of Chlorella cells, juvenile daphniids were observed. Using a plastic dropper with a tipped end, they were transferred into a clean 250 mL glass beaker filled with desalinated bottled commercial drinking water with a few drops of Chlorella culture cells to establish a laboratory culture. Specimens from this laboratory culture were studied below.
For the morphological analysis, available specimens of Daphnia (Ctenodaphnia) were selected from preserved samples under a binocular stereoscopic microscope LOMO (LLC LOMO-Microsystems, St. Petersburg, Russia) and studied in their entirety under an optical microscope OLYMPUS BX41 (Olympus Corporation, Tokyo, Japan) in a drop of glycerol–ethanol or a glycerol–formaldehyde mixture. Then at least 10 parthenogenetic females and five adult males from each locality (if available) were dissected under a stereoscopic microscope for the study of appendages and postabdomen in a drop of glycerol using tungsten needles sharpened in concentrated alkali solution using the electrogalvanic method (Frey, 1986, Kořínek, 1999). The line drawings were prepared using a camera lucida attached to an Olympus BX 41. Some specimens were dehydrated and dried according to a standard protocol [42], coated with gold in Q150R ES Plus (Quorum Technologies Ltd., East Sussex, UK) and investigated under a scanning electron microscope TESCAN MIRA 3 LMH (TESCAN, Brno, Czech Republic). For the morphological description we used terminology summarised and discussed by Kotov [42].

2.2. Abbreviations in Illustrations and Text

I–V = thoracic limbs I–V; e1–e5 = endites 1–5 of thoracic limbs; ejh = ejector hooks on limb I; epp = epipodite; ext = exopodite; IDL = inner distal lobe of limb I; ODL = outer distal lobe of limb I; pep = preepipodite; s = sensillum.

2.3. Genetic Analysis

DNA extraction was performed using the specimens initially identified by their morphological character. Genomic DNA was extracted from single adult parthenogenetic females using the Wizard Genomic DNA Purification Kit (Promega Corp., Madison, WI). We used as genetic markers: (1) the 5′-fragment of the first subunit of mitochondrial cytochrome oxidase (COI), (2) the fragment of 16S rRNA gene (16S), and (3) the 5′-fragment of the mitochondrial 12S rRNA gene (12S). Amplification was performed using earlier-published protocols [10,40]. Each PCR product was sequenced bi-directionally on the ABI 3730 DNA Analyzer (Applied Biosystems) using the ABI PRISM BigDye Terminator v.3.1 kit at the Syntol Co, Moscow, Russia. Initial analysis of the chromatograms, formation of contigs and their subsequent editing was conducted using the Sanger Reads Editor in the Unipro uGENE v.42 [43]. Sequences were verified by BLAST comparisons with published cladoceran sequences in the NCBI BLAST nr/nt database [44]. The sequences from this study were submitted to the NCBI GenBank database (accession numbers ON312918-ON312919, ON320393-ON320394, ON320535, and ON320536-ON320554) (Table S1).
The alignment was carried out using the MAFFT v.7 algorithm [45]. Substitution models were selected using ModelFinder v.1.6 [46] at the Center for Integrative Bioinformatics Vienna, Austria web-server [47]. For the COI locus, the substitution model was identified for each (1st, 2nd, 3rd) nucleotide position in the codon. Substitution models were selected based on minimal values of the Bayesian information criterion, BIC [48]. All selected models demonstrated convergence according to the BIC and AICc information criteria, providing additional evidence for model fit. The following models were selected: COI 1st—TIM3e + G4, COI 2nd—HKY + F + I + G4, and COI 3rd—HKY + F + R2, 12S—TIM2 + F + G4, 16S—TVM + F + I + G4. Phylogenetic reconstructions based on the maximum likelihood (ML) and Bayesian (BI) methods were made based on “unlinked” data on each locus and the nucleotide position in each codon, then a consensus tree for all “unlinked” dataset was built. Joining of all sequences into a single dataset and the formation of the nexus files was performed in the SequenceMatrix v.1.7 [49].
ML analysis was conducted using IQ-TREE v.1.6.9 [50] at the Center for Integrative Bioinformatics Vienna web-portal, Austria. Each set of sequences was analysed based on the best model that was found automatically by W-IQ-TREE [47]. To estimate the branch support values, we used 1k replicas of the bootstrap test in ultra-fast bootstrap [51]. As a topology test, we used the SH-aLRT test algorithm [52] in the W-IQ-TREE server.
For BI analysis we used the multi-taxon coalescence model “star” [53] in the software packages BEAST2 v.2.6 [54] with all of the parameters of the substitution model determined using BEAUti [55]. In each analysis, we conducted six independent runs of the Markov chain Monte-Carlo (MCMC, 20M generations, with a selection of each 10 k generation). Sequences of D. longispina and D. pulex from the NCBI GenBank were used as outgroups. The effectiveness of the MCMC runs, taking into consideration the estimations of the effective size (ESS) for all parameters higher than 200, was controlled in Tracer v.1.7 [56]. After uniting the MCMC runs using LogCombiner (part of BEAST2), a consensus tree was obtained in TreeAnnotator (part of BEAST2) with a burn-in rate of 25%. Posterior probabilities were used as support values following the recommendations of Drummond and Bouchkaert [57]. Since the main clades for BI and ML were congruent, we presented the ultrametric BI trees, with branch support for key nodes.
For the estimation of possible divergence ages of different clades, we used the molecular clocks with paleontological calibration [58], as this method has advantages when compared with analytical methods based on complicated mathematical models. We used the calibration point of Cornetti et al. [59]: Daphnia/Ctenodaphnia divergence point with 15% standard deviation. The age of lineage divergence was estimated based on the optimised relaxed clock model in the ‘ORC’ package [60] for BEAST2 with the Yule model of speciation as maximally adequate for the data on several species [61]. Further analysis was conducted according to Barrido-Sottani et al. [62].
Unfortunately, we did not have available molecular samples on D. similoides from India. Some short 12S sequences of this species were taken from the publication of Popova et al. [40], but due to their length they were not previously deposited to the GenBank. A median joining 12S haplotype network was constructed in popART v.1.7 [63] using these sequences.
The combined species tree estimation and species delimitation analysis based on several loci was conducted in STACEY v.1.2 (Species Tree And Classification Estimation, Yarely) [64] for BEAST2, as this method was regarded as most adequate for Daphnia when compared to other delimitation methods [21]. As it was demonstrated previously [65], ploidy value could be critical for a good correspondence of morphological and genetic “taxonomic units” in STACEY, while the priors could have wide ranges. We chose for our analysis the ploidy = 1 and the Yule speciation model, while other parameters were kept by default. Final genealogical relationships were estimated using STACEY in four independent runs (50M generations, with a selection of each 10 k generation with a preliminary burn-in of 10%) with effectiveness control in Tracer. A consensus tree based on the maximum clade credibility (MCC) was obtained in TreeAnnotator with a burn-in of 50% of trees. Delimitation of the trees based on STACEY results was made in speciesDA [64] ignoring first half of the trees.
MEGA-X software [66] was used to calculate genetic distances. We selected “simple” p-distances as more preferable for DNA barcoding [67], as there was no significant difference between uncorrected and corrected substitution models in the case of a sufficiently large dataset [68].

3. Results

3.1. Taxonomy and Morphological Account

Order Anomopoda Sars, 1865
Family Daphniidae Straus, 1820
Genus Daphnia O.F. Müller, 1776
Subgenus Daphnia (Ctenodaphnia) Dybowski & Grochowski, 1895
Daphnia (Ctenodaphnia) arabica Neretina, Al Neyadi & Hamza sp. nov.
Zoobank taxon ID. urn:lsid:zoobank.org:act:2E3DD8E7-D7BA-4420-9B3A- 50432FB51E98. The electronic version of this article in Portable Document Format will represent a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. The LSID for this publication is: urn:lsid:zoobank.org:pub:A4A3415D-857E-42E5-9103-B8D48AC60832. The online version of this work is archived and available from the following digital repository: MDPI Water.
Etymology. This species is named after the Arabian Peninsula, where the taxon was found.
Type locality. Al Shuwaib Dam (N 24.771°, E 55.80146°), near Al Ain city, Abu Dhabi Emirate, the United Arab Emirates.
Holotype. An adult parthenogenetic female preserved in 96% alcohol, deposited to the Invertebrates collection of the Environmental Agency of Abu Dhabi, accession number ICEAD-WC1-01.
Allotype. An adult male preserved in 96% alcohol, deposited to the Invertebrate collection of Zoological Museum of M.V. Lomonosov Moscow State University, MGU Ml 256.
Paratypes. Many parthenogenetic, ephippial females and males in the Invertebrates collection of the Environmental Agency of Abu Dhabi, accession number ICEAD-WC1–02; many parthenogenetic, ephippial females and males, MGU Ml 257 10 ephippial females MGU Ml 258. 10 males, MGU Ml 259.
Description.
Adult parthenogenetic female. The body was almost transparent, with body height/length (without caudal spine) = 0.56. In lateral view, the body was subovoid, with a maximum height in the middle of valves (Figure 1a). In dorsal view, the body was laterally compressed, with a low dorsal crest. The dorsal margin of valves was slightly raised above head level, and regularly convex; a depression between the head and the rest of body was prominent. In the largest individuals, there was a posterodorsal angle of the valve with a relatively short (length being about 0.1 times the body length) caudal spine.
The head was relatively large (length being about 0.3 times the body length), with a prominent pointed rostrum with a pointed tip, not subdivided into two lobes by a ‘line’ of pre-rostral fold (Figure 1c). The posterior margin of head had a mound between antennae I, and prerostral fold was not expressed; the head was without any pre-ocular and post-ocular depressions. The eye capsule was located below the level of the anteriormost point of the head. The compound eye was relatively small (with a diameter of about 0.15 times the head length), the ocellus was very small, located closer to the compound eye than to the base of antenna I. There was a head shield with slightly projected, sharp fornices, and a projection from the valves penetrates to about 0.3–0.5 length of the former. The labrum was large, sub-rectangular, densely setulated (Figure 1d). The setulae of the distal labral plate was organised into series.
The valve was subovoid (Figure 1e), with its posteroventral portion having internally located setae and rows of setules between them (Figure 1f,g), and a group of relatively long setulae (length being about 0.1–0.2 times the body height) in the middle of the ventral margin (Figure 1h). It had a caudal spine covered by small denticles; they also occupied more than half of the dorsal and ventral valve margin from the posterior end (Figure 1a).
The abdomen was short, with two basalmost (anteriormost) projections that were long and curved; the third segment with a low mound; the fourth segment without a projection (Figure 2a and Figure 3a,b). The postabdomen was elongated, narrowing in its distal portion, with a straight ventral margin. The preanal margin was long, and the preanal angle smooth postanal angle was not pronounced. Postanal and anal portions bore marginal spines (Figure 2b and Figure 3a–e). The postabdominal claw was regularly curved, with a pointed tip (Figure 2b and Figure 3a–e). On the outer side of claw, there were three successive pectens along the dorsal margin. The first (proximal) pecten and the second (medial) one was composed of thin teeth; the third one was composed of numerous, fine setules, and their row almost reached the claw tip. The postabdominal seta was as long as the preanal margin, and its distal segment was slightly shorter than the basal one (Figure 1a).
Antenna I was a mound bearing nine aesthetascs of the same length and had antennular sensory seta that rose from the base of the antenna I body (Figure 1i); aesthetascs projected post-ventrally and their tips did not reach the tip of the rostrum. Antenna II had a narrow coxal part, with a basal segment being elongated and having well-developed distal sensory setae on the posterior margin (Figure 2c). Antennal branches were elongated; the endopod with three segments was almost subequal in length to the exopod with four segments, each of them having a series of minute denticles. Antennal setae formula: 0-0-1-3/1-1-3. Apical segments bore rudimentary spines; the spine on the second exopod segment was small (length being about 0.2 times the next-segment length) and thick. Swimming setae with basal and distal segments were covered by long setules.
Limb I was without an accessory seta (Figure 2d,e); outer distal lobe (ODL) carried a long (longer than any other setae) seta bilaterally armed distally with short setules, and a short seta. IDL (endite 4) had a single, long (only somewhat shorter that the ODL seta) anterior seta 1 covered by short setules distally. Endite 3 had a long (only somewhat shorter than seta 1) anterior seta 2 armed with minute setules and two posterior setae (a,b). Endite 2 had a long (as long as seta 2) anterior seta 3 and two posterior setae (c,d). Endite 1 had a long (longer that half the length of seta 3) anterior seta 4 and four posterior setae (e–h). It had two setulated ejector hooks of remarkably different length (Figure 2d: ejh).
Limb II had an exopodite (Figure 4: ext) as a large lobe carrying two soft and setulated seta. It had four endites (Figure 4a: e1–e5) altogether armed by five setae: anterior (stiff and unilaterally setulated) seta 1 and four posterior setae (Figure 4a: a–d). The gnathobase had two rows of setae, four anterior setae (Figure 4a,b: 1–4) and 18 posterior setae on the gnathobasic filter plate (Figure 4a,b: a–q).
Limb III had an elongated preepipodite (Figure 4d: pep) and subglobular epipodite (Figure 4d: epp) and a large (its length being about half of the limb length), flat exopodite (Figure 4d: ext) carrying four distal and two lateral setae. Endite 4 bore a single, long anterior seta (Figure 4e: 1) and a posterior seta (Figure 4e: a). Endite 3 bore a single anterior seta 2 and a single posterior seta. Endite 3 had a single anterior (Figure 4e: 2) and single posterior (Figure 4e: b) seta. Endite 2 had a rudimentary anterior seta 3 and two posterior setae (Figure 4e: c,d). Endite 1 had one long anterior (Figure 4e: 4) seta and four posterior setae (Figure 4e: e–h). The rest part of the limb was a gnathobase, bearing numerous filtering setae and four rudimentary anterior setae, with three of them transformed into sensillae (Figure 4e: s).
Limb IV had a large (its length being about half of its limb length) ovoid preepipodite (Figure 5a: pep), an ovoid epipodite (Figure 5a: epp) and a wide, flat exopodite (Figure 5a: ext). Similar to the previous limb, it bore four distal setae (the second seta with minute setules distally), and two lateral setae. The inner distal portion consisted of completely fused endites, an inner margin with a gnathobasic filter plate consisting of two anterior and numerous posterior filtering setae.
Limb V (Figure 5c–e) had a small (smaller than epipodite), setulated preepipodite and subovoid epipodite. The exopodite was triangular, with two long (longer than the exopodite body itself) setae and a short (length being about 0.15 of the distal exopodite margin length) and thin seta in the middle of the outer margin (Figure 5c–e: arrows), the latter being longer than marginal setules. The inner limb portion was an ovoid flat lobe, with a setulated inner margin bearing a single long seta.
Juvenile female. Body was subrectangular, with a straight posterior margin, a long (in the small-sized individuals the length was about 0.3 times the body length) caudal spine and the posterior half of the ventral valve margin was covered by spinules (Figure 1b). The head had a straight ventral margin, short rostrum and convex dorsal margin.
Ephippial female. The body was the same as the parthenogenetic female, but dorsal portion of the valves was modified into an ephippium (Figure 6a,b, Figure 7 and Figure 8) and the dorsal margin was almost straight. The ephippium was darkly pigmented, “D-shaped” in Hudec’s terms [69], with two resting eggs and egg chambers separated from each other; most of the ephippium body was covered with reticulation. The caudal spine and the whole postero-dorsal part of the valves was incorporated into the ephippium.
Adult male. The body was low; the dorsal margin was straight, not elevated above head level; the depression between the head and valves was absent; the postero-dorsal angle was distinct, with a relatively long (length being about 0.3 times the body length) caudal spine (Figure 6d and Figure 9a).
The head had a short (shorter than antenna I diameter) smooth rostrum directed ventrally (Figure 6e and Figure 9b,c); the region of antenna I joint had a prominent depression. The ventral margin of the head was slightly concave. The supraocular depression was absent; the eye was large, with a small ocellus located at the middle of the distance between an eye and bases of antennae I. The labrum was the same as the female (Figure 6f).
There was a valve with an anteroventral angle somewhat prominent ventrally; the ventral margin had a row of numerous long setae (Figure 6g); the posteroventral portion of the valve had shorter setae and setules between them and was located on the inner side of the valve.
The abdomen had almost smooth abdominal processes. The postabdomen had a structure in general similar to the female, but the preanal margin was shorter and the postanal angle was expressed (Figure 6h, Figure 9d–f and Figure 10a). The anal margin had 4–6 paired teeth increasing in size distally and the preanal margin had a series of fine setules. The gonopore opened subdistally, without general papilla. Postabdominal claws had a basal pecten of fine denticles; the second pecten had more robust denticles; the third pecten consisted of fine setules.
Antenna I was long (its length was the same as the head length) and relatively straight, with a very small (its length was smaller than the diameter of antenna I) antennular seta, located far from the distal end of antenna I body (Figure 9g,h and Figure 10b–d). The aesthetascs were of the same length. Male seta were on top of the distal process, long and bisegmented and its distal segment was densely setulated. Antenna II (Figure 9i) was the same as the female.
Limb I had a large, cylindrical outer distal lobe, bearing a rudimentary seta and a very large seta supplied with minute setulae distally (Figure 10e,f). The inner distal lobe had a curved copulatory hook and two setae of different sizes; endite 3 had four setae. Limb II had a long seta 1 (Figure 10h). Limb V was the same as the female (Figure 10i).
Size. The parthenogenetic female was 0.69–1.9 mm; the ephippial female was up to 1.6 mm; the male was 0.9–1.3 mm in length.
Distribution. To date, D. arabica sp. nov. was found only in a single locality in the United Arab Emirates.
Differential diagnosis.D. arabica sp. nov. is a member of the D. (C.) sinensis group within the D. (C.) simils species complex [40]. D. simils species complex differs from other Palaearctic taxa of D. (Ctenodaphnia) by having a very small or fully reduced seta in the middle of the external margin of exopodite V (while all other well-studied species have a well-developed seta there). Moreover, D. (C.) similis complex has no head plate with “crown of thorns” in contrast to the D. (C.) atkinsoni group and D. (C.) triquetra Sars, 1903; it has no lateral keels on the head shield in contrast to D. (C.) magna Straus, 1820; it has relatively developed antenna I in contrast to the D. (C.) carinata complex, D. (C.) hispanica Glagolev & Alonso, 1990, D. (C.) fusca Gurney, 1907 and D. (C.) chevreuxi group, while its antenna I is not as long as that of D. (C.) mediterranea Alonso, 1985; it has no spine-like fornices and a spine-like helmet as characterised by D. (C.) lumholtzi Sars, 1885; it has a caudal spine in contrast to D. (C.) tibetana (Sars, 1903).
Differentiation of species within the D. (C.) similis complex is based mainly on ephippium and male characters. The D. (C.) sinensis species group (within the latter complex) could be differentiated easily from D. (C.) similis s. str. based on its “D-shaped” ephippium (in contrast to the “O-shaped” ephippium in the latter) and the teeth on the male postanal margin transformed into fine setules (in contrast to non-reduced teeth in the latter).
All three earlier-derived members of the D. (C.) sinensis group (D. similoides, D. inopinata and D. arabica sp. nov.) could be differentiated from D. (C.) sinensis based on (1) a relatively small compound eye not occupying the whole anterior portion of the head and not making a well-developed ocular dome as in the latter and (2) full absence of a seta in the middle of the exopodite V outer margin. However, further differentiation is based on fine male characters. In contrast to D. (C.) similoides, D. (C.) arabica sp. nov. has a seta in the middle of the exopodite V margin that is longer than marginal setules. Note that Popova et al. [40] concluded that D. (C.) inopinata differed from D. (C.) similoides in the presence of this seta, but this is not true (Figure 11, e–g): in reality D. (C.) similoides also has this seta there, but it is shorter than the marginal setules, and it is longer than the marginal setules in D. (C.) inopinata and D. (C.) arabica sp. nov.
D. (C.) arabica sp. nov. also differs from D. (C.) similoides in the following characteristics: (1) the female rostrum is directed posteriorly; (2) seta 1 on the inner-distal portion of limb II is relatively short (its length is two-thirds of the soft seta b length); (3) the smooth male rostrum; and (4) the very fine setules on the postanal portion of the male postabdomen replacing the anal teeth. D. (C.) arabica sp. nov. differs from D. inopinata in the following characteristics: (1) the slightly concave ventral head margin and rostrum directed ventrally in the adult male; (2) almost all abdominal projections being smooth in the adult male, while at least the projection on the second abdominal segment is relatively long in D (D.) inopinata; (3) also a projection of the posterior margin of the female head is lying between antennae I in the former, while dorsally to it in the latter.

3.2. Genetic Account

Estimates of evolutionary divergence over sequence pairs between major clades of Daphnia using COI gene sequences are represented in Table 1. Different pairs of species demonstrate a very different level of genetic differentiation. Note a very high level of differentiation between the similis and sinensis groups and a high level of genetic diversity within each group. D. arabica sp. nov. differs from other groups by at least 9%; this means that it could be recognised as a “good” species according to Hebert et al. [70]. All major clades below also represent “good” species.
An ultrametric tree based on three mitochondrial genes (12S, 16S and COI) is represented in Figure 12. Nineteen well-supported OTUs (=major clades) were selected by STACEY. The first three OTUs (1–3) correspond to D. sinensis; note that sequences from Ethiopia and Iran made separate clades (2 and 3). The aforementioned three clades, plus clade 4 (D. arabica sp. nov.) and clade 5 (D. inopinata) make a well-supported major clade, the D. sinensis species group. The next major clade was the D. lumholtzi species group, uniting clades 6 (D. lumholtzi s. str. from Australia) and 7 (D. cf. lumholtzi from North America, but note that the latter is an invader from Africa). Clade 8 is D. similis s. str. Clades 1–8 make a superclade moderately supported by UFboot and well-supported by SH-aLRT tests, D. similis complex. The group is paraphyletic in terms of morphology because it contains D. lumholtzi, having a specific morphology and does not belong to the similis-like taxa.
Other taxa are not so important for the purposes of this study, and they are only listed below: Daphnia magna s. str. (9); well-supported D. carinata group consisting of five taxa in our dataset: D. carinata (10), D. longicephala (11), D. nivalis (12), D. cephalata (14), D. salinifera (14); well-supported D. exilis group consisting of two taxa: D. exilis (with D. spinulata as its junior synonym) and D. cf. similis from North America; D. atkinsoni (17), D. barbata (18) and D. dolichocephala (19).
Keeping in mind the calibration point of the Daphnia/Ctenodaphnia split at the Jurassic/Cretaceous boundary, we can roughly estimate the time of differentiation of the D. similis complex as a Upper Cretaceous (Figure 12); split of D. similis s. str. vs. other clades (1–7) as well as D. lumholtzi vs. other clades (1–5) of this complex as Palaeocene, split of the clades in the D. sinensis complex as Oligocene-Miocene, differentiation of subclades (1–3) within D. sinensis group as ca. Oligocene and differentiation of the terminal clades within D. sinensis s.str. as Pleistocene.
The 12S haplotype network (Figure 13) is constructed based on short fragments, it means the number of substitutions have a limited significance for the understanding of the species delimitation. D. similoides, D. inopinata and D. arabica sp. nov. are separated by 4–6 substitutions, but it is not reason to doubt their status as a separate taxa. They form a separate cluster interconnected to the cluster of D. sinensis through the Ethiopian haplotype which is also interconnected with the Mediterranean and mainly Mediterranean haplotypes, one of which then interconnected to the haplotypes from North-East Asia and India. The Iranian haplotype is separated from other D. sinensis haplotypes by at least four mutations, as observed in its specific position on the tree also (Figure 12 and Figure 13). Note that the Middle East, North Africa and India are rich in haplotypes which are endemic to particular regions. In contrast to D. similoides, D. inopinata and D. arabica sp. nov., D. sinensis s. str. has several widely distributed haplotypes separated by single mutations. The network of D. sinensis group corresponds in general to the tree in Figure 12. Other species are well-separated in the network from the D. sinensis group, and its closest congener is D. lumholtzi (as in the tree), while D. similis is grouped with D. cf. similis from North America (=D. exilis group) and D. magna.

4. Discussion

4.1. Morphology and Species Distribution

Our morphological account demonstrates that the D. (C.) similis species complex could clearly be separated into D. (C.) similis s.str. and the D. (C.) sinensis species group. Unfortunately, ideas on the distribution of D. (C.) similis [28] are strongly outdated, and its real geographic range in the Palaearctic is unknown. The ideas on the distribution of D. (C.) sinensis s. str. are more obvious: this taxon is very common in the Far East (from Russian Primorye to South China), Mongolia, South Siberia, Iran, Azerbaijan, the southern portion of European Russia, the whole of Africa [20,40,71]. According to GenBank sequence MT709058, it is also present in India (its exact locality was not represented, but the specimen probably originated from Kerala), although the taxon is rare in the tropical latitudes of Eurasia. Therefore, we can confirm that D. (C.) sinensis is widely distributed in Africa and Asia. Moreover, the ephippia of D. (C.) sinensis are found in a Lower Pleistocene palaeolocality in Transbaikalian Siberia [72].
Three other species from the D. (C.) sinensis group are locally distributed and the main characteristics distinguishing them from D. (C.) sinensis s. str. are plesiomorphies, suggesting their earlier deviation from the D. (C.) sinensis lineage. As a result, D. (C.) sinensis could be regarded as a very successful crown-group, while other members could be regarded as an earlier-derived “phylogenetic relicts” sensu Grandcolas [73]. These water fleas are large cladocerans, but their differences are minute and mainly based on the male characteristics. However, this is common among the cladocerans and could be explained by a deep morphological stasis [72].

4.2. Tree and Network Analysis

Our tree agrees in its general topology with previously published trees based on same set of mitochondrial genes [22,40]. However, we added more taxa to the analysis, i.e., from the sinensis-group (the latter was represented in the tree of Adamowicz et al. [22] by a single sequence: D. gr. similis sp. 2 from Europe which belonged to the subsequently described D. inopinata [40]). According to Popova et al. [40], D. barbata was grouped with D. similis and D. sinensis, but support of this grouping was very low, and now it is obvious that D. barbata is not related to D. sinensis.
Finally, our tree corresponded in its general topology with both trees based on genomic data by Cornetti et al. [59] except in several details: the position of the D. carinata group (our clades 10–14), which is a sister group of D. similis + D. sinensis + D. lumholtzi clade according to Cornetti et al. [59] with a strong support in the tree based on 636 nuclear genes; and the position of D. magna, which is a sister group of D. exilis group according to Cornetti et al. [59] and is a sister group of D. similis complex + D. lumholtzi clade (1–8) in our tree.
The similis complex (our clades 1–8) is well-supported in all the trees of [59], although D. lumholtzi is found by them to be an earlier-derived taxon, a sister group to D. similis + D. sinensis clade. We fully agree with Cornetti et al. [59] that D. similis complex (distributed in the eastern hemisphere) is not related to the D. exilis-group (distributed in the western hemisphere). Here we discuss only the former group and only events in the eastern hemisphere. Based on both our tree and the trees of Cornetti et al. [59], we can conclude that the D. lumholtzi group is either a member of the D. similis complex or its closest congener, and we discuss the former group here as well.
Based on Figure 12, we can conclude that clades 4, 6 and 7 are apparently “Gondwanan”. The origin of clade 5 (D. inopinata) is dubious; it was found to date in a single locality, a pond in a military training ground in Germany, and regarded as an anthropogenically-mediated invader from an unknown region [40,74]. We therefore suggest that the probability of its origin being from a “Gondwanan” territory is very high. Moreover, the earlier-derived clades of D. sinensis are also from the Gondwanan territory (2) or closest territory of the Middle East (3). We can hypothesise that the region of the Middle East and North Africa was the center of the D. sinensis group dispersion after the previous Gondwanan group differentiation in the Late Mesozoic period and D. lumholtzi is a taxon of apparently Gondwanan differentiation (in the territory of future North Africa and the Arabian Peninsula and, possibly, India which was already relatively far away from Africa at that time). Our molecular clock estimations suggest the separation of the major clade uniting the terminal clades 1–7 around the Mesozoic/Caenozoic boundary, which is consistent with the aforementioned assumption.
Clades of the sinensis group (clades 1–5) are younger and their separation cannot be explained in terms of a continental drift; it happened when the continents had almost reached their recent positions. Based on the recent distribution of earlier-derived groups and their endemic status, we can draw the dispersion center as Mediterranean-Middle East-North Africa. The haplotype network confirms such a hypothesis: just in these regions, haplotypes are endemic and separated by more substitutions from each other when compared to the “core” of the sinensis-group. Moreover, they are connected to the haplotypes of D. sinensis also distributed in the same region. Based on our molecular clocks, we can suggest that such differentiation took place in the Oligocene-Miocene period. It was a remarkable time of climatic changes on the planet which led to a mass extinction and re-distribution of the cladoceran taxa, i.e., premature survival in the subtropical regions and neighbouring regions of temperate zone [21,75]. The mass extinction was even reinforced during the coldest and arid phases of the Pleistocene period. As we can assume, the structure of the “right” side of our network (D. similoides, D. inopinata and D. arabica sp. nov.) reflect a Late Caenozoic extinction of this group. They survived in the regions with different climates, from mild Indian localities to Arabian deserts.
Apparently, strong climatic changes i.e., a strong Pleistocene aridisation of North Africa, the Arabian Peninsula and the Middle East and possible glaciation in mountain areas of North Africa [76,77,78,79] probably led to a mass extinction of the cladocerans there. Note that the chance of finding many additional populations of our daphniids in the desert and arid regions of the Middle East is relatively small.
We believe that the Middle East and then the Mediterranean Region became a center of subsequent dispersion of D. (C.) sinensis (Figure 12, clades 1–3) through the whole of Eurasia and Africa during the Miocene and subsequent epochs. The exact timing of such events is not clear. However, we do not have the full set of genes for populations studied by Ma et al. [80]. These authors have estimated the time of the sinensis-group differentiating as c.a. 25 MYA (which is even older than our estimation!) and the time of the differentiation of populations from Eastern and Western China as c.a. 12 MYA (Middle Miocene, older than our estimation). Moreover, they demonstrated a strong haplotype diversity in China and related it to the uplift of the Qinghai-Tibetan Plateau. Such data do not contradict our hypothesis. According to our molecular clocks, the differentiation of clade 1 took place, most probably, in Pleistocene, in the late epoch, but we did not analyse the Chinese sequences here. Moreover, the central haplotype H1 of Ma et al. [80] occurs both in China and European Russia (the Black Sea basin) which could be explained, most probably, by a very young (Pleistocene or younger) differentiation. The scenario of a very recent anthropogenic invasion could not be fully rejected, but it is difficult to suggest the vector of such invasion.
Another ctenodaphniid, D. magna [17], rapidly colonised most of the territory of Western Eurasia up to Central Siberia during Pleistocene period, where it formed a zone of secondary contact with the “American” clade of D. magna having a completely different evolution history and monopolising a significant portion of East Asia [33], including lowland China and Tibet [81]. Such pattern is found in some other well-studied cladocerans groups [27,82,83]. In contrast, D. sinensis did not meet any congener species during its movement north and east, and its populations could be found even in the Pacific coast of Eurasia.
Even India (taking into consideration the sequence directly submitted to the NCBI GenBank by Indian investigators without information on its exact locality) was colonised by D. sinensis (although it was already populated by D. similoides), but the exact timing of such event is unknown. We cannot exclude the possibility that the Indian population represented in the GenBank has appeared as a result of a very recent human-mediated introduction, as it belongs to a widely distributed East Asian haplotype. Such recent invasions are very common among the daphniids including D. (Ctenodaphnia) [33,84,85].
At present, D. sinensis is very common in East Asia [40]. Moreover, this is a single species of Daphnia (Ctenodaphnia) in many regions of the Far East [86]. However, we hypothesise that all of these populations have appeared as a result of a colonisation from the North Africa-Middle East-Mediterranean Region. We need to search for fossil records to check this hypothesis. To date, D. similis ephippia were found in a single Pleistocene (older than 1.5 MYA) locality in Transbaikalia [72], while any records of D. sinensis are unknown.

5. Conclusions

Our scheme of the D. sinensis group dispersion has a well-known analogue: it is similar to that suggested for earlier human migration from Africa through the Arabian Peninsula and the Middle East to everywhere in Eurasia [87,88], although, the daphniids are strongly older in the time of their differentiation, and, most likely, they invaded Northern Eurasia earlier when compared to hominids.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w14152350/s1, Table S1: Sequences used in this study.

Author Contributions

Conceptualisation, W.H. and A.A.K.; methodology, A.N.N. and D.P.K.; software, D.P.K.; formal analysis, S.E.S.A.N., A.N.N., K.M.A.A. and W.H.; investigation, W.H., S.E.S.A.N., K.M.A.A., A.N.N. and D.P.K.; resources, K.M.A.A. and S.E.S.A.N.; data curation, S.E.S.A.N., A.A.K.; writing—original draft preparation, W.H., A.N.N. and A.A.K.; writing—review and editing, W.H. and A.A.K.; visualisation, A.N.N. and D.P.K.; supervision, W.H.; project administration, W.H. and A.A.K.; funding acquisition, W.H. and A.A.K. All authors have read and agreed to the published version of the manuscript.

Funding

All works in UAE are self-supported by Waleed Hamza, Biology Department, UAEU; phylogeographic studies are supported by the Russian Science Foundation (grant 18-14-00325).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The sequences from this study were submitted to the NCBI GenBank database (accession numbers ON312918-ON312919, ON320393-ON320394, ON320535, ON320536-ON320554).

Acknowledgments

The authors would like to thank Khalifa Center for Genetic Engineering and Technology, United Arab Emirates University for the in-kind support for conducting of the DNA extraction and PCRs. Many thanks to S. Muzaffar for linguistic corrections of the earlier draft and R.J. Shiel for proofreading the final version.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Leveque, C.; Oberdorff, T.; Paugy, D.; Stiassny, M.L.J.; Tedesco, P.A. Global diversity of fish (Pisces) in freshwater. In Freshwater Animal Diversity Assessment; Balian, E.V., Leveque, C., Martens, K., Segers, H., Eds.; Springer: Dordrecht, The Netherlands, 2008; pp. 545–567. ISBN 978-1-4020-8258-0. [Google Scholar]
  2. Su, G.; Logez, M.; Xu, J.; Tao, S.; Villeger, S.; Brosse, S. Human impacts on global freshwater fish biodiversity. Science 2021, 371, 835–838. [Google Scholar] [CrossRef]
  3. Adamowicz, S.J.; Purvis, A. How many branchiopod crustacean species are there? Quantifying the components of underestimation. Glob. Ecol. Biogeogr. 2005, 14, 455–468. [Google Scholar] [CrossRef]
  4. Forro, L.; Korovchinsky, N.M.; Kotov, A.A.; Petrusek, A. Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia 2008, 595, 177–184. [Google Scholar] [CrossRef]
  5. Balian, E.V.; Segers, H.; Leveque, C.; Martens, K. The freshwater animal diversity assessment: An overview of the results. Hydrobiologia 2008, 595, 627–637. [Google Scholar] [CrossRef]
  6. Hebert, P.D.N.; Cywinska, A.; Ball, S.L.; deWaard, J.R. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 313–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Elias-Gutierrez, M.; Hubert, N.; Collins, R.A.; Andrade-Sossa, C. Aquatic organisms research with DNA barcodes. Diversity 2021, 13, 306. [Google Scholar] [CrossRef]
  8. Ebach, M.C.; Holdrege, C. DNA barcoding is no substitute for taxonomy. Nature 2005, 434, 697. [Google Scholar] [CrossRef] [Green Version]
  9. Garibian, P.G.; Neretina, A.N.; Taylor, D.J.; Kotov, A.A. Partial revision of the neustonic genus Scapholeberis Schoedler, 1858 (Crustacea: Cladocera): Decoding of the barcoding results. PeerJ 2020, 8, e10410. [Google Scholar] [CrossRef]
  10. Neretina, A.N.; Karabanov, D.P.; Sacherova, V.; Kotov, A.A. Unexpected mitochondrial lineage diversity within the genus Alonella Sars, 1862 (Crustacea: Cladocera) across the Northern Hemisphere. PeerJ 2021, 9, e10804. [Google Scholar] [CrossRef]
  11. Fernando, C.H.; Paggi, J.C.; Rajapaksa, R. Daphnia. Memorie Dell’ Istituto Italiano di Ldrobiologia; Peters, R.H., De Bernardi, R., Eds.; Istituto Italiano di Idrobiologia: Pallanza, Italy, 1987. [Google Scholar]
  12. Miner, B.E.; de Meester, L.; Pfrender, M.E.; Lampert, W.; Hairston, N.G. Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proc. R. Soc. Lond. B Biol. Sci. 2012, 279, 1873–1882. [Google Scholar] [CrossRef] [Green Version]
  13. Smirnov, N.N. Physiology of the Cladocera, 2nd ed.; Academic Press: Amsterdam, The Netherlands, 2017; ISBN 9780128051948. [Google Scholar]
  14. Taylor, D.J.; Finston, T.L.; Hebert, P.D.N. Biogeography of a widespread freshwater crustacean: Pseudocongruence and cryptic endemism in the North American Daphnia laevis complex. Evolution 1998, 52, 1648–1670. [Google Scholar] [CrossRef] [PubMed]
  15. Weider, L.J.; Hobaek, A.; Colbourne, J.K.; Crease, T.J.; Dufresne, F.; Hebert, P.D.N. Holarctic phylogeography of an asexual species complex: I. Mitochondrial DNA variation in arctic Daphnia. Evolution 1999, 53, 777–792. [Google Scholar] [CrossRef] [PubMed]
  16. Weider, L.J.; Hobaek, A.; Hebert, P.D.N.; Crease, T.J. Holarctic phylogeography of an asexual species complex: II. Allozymic variation and clonal structure in arctic Daphnia. Mol. Ecol. 1999, 8, 1–13. [Google Scholar] [CrossRef]
  17. de Gelas, K.; de Meester, L. Phylogeography of Daphnia magna in Europe. Mol. Ecol. 2005, 14, 753–764. [Google Scholar] [CrossRef] [PubMed]
  18. Petrusek, A.; Cerny, M.; Mergeay, J.; Schwenk, K. Daphnia in the Tatra Mountain lakes: Multiple colonisation and hidden species diversity revealed by molecular markers. Fund. App. Lim. 2007, 169, 279–291. [Google Scholar] [CrossRef]
  19. Ma, X.; Petrusek, A.; Wolinska, J.; Giebler, S.; Zhong, Y.; Yang, Z.; Hu, W.; Yin, M. Diversity of the Daphnia longispina species complex in Chinese lakes: A DNA taxonomy approach. J. Plankton Res. 2015, 37, 56–65. [Google Scholar] [CrossRef] [Green Version]
  20. Wu, J.; Wang, W.; Deng, D.; Zhang, K.; Peng, S.; Xu, X.; Zhang, Y.; Zhou, Z. Genetic diversity and phylogeography of Daphnia similoides sinensis located in the middle and lower reaches of the Yangtze River. Ecol. Evol. 2019, 9, 4362–4372. [Google Scholar] [CrossRef] [Green Version]
  21. Kotov, A.A.; Garibian, P.G.; Bekker, E.I.; Taylor, D.J.; Karabanov, D.P. A new species group from the Daphnia curvirostris species complex (Cladocera: Anomopoda) from the eastern Palaearctic: Taxonomy, phylogeny and phylogeography. Zool. J. Linn. Soc. 2021, 191, 772–822. [Google Scholar] [CrossRef]
  22. Adamowicz, S.J.; Petrusek, A.; Colbourne, J.K.; Hebert, P.D.N.; Witt, J.D.S. The scale of divergence: A phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus. Mol. Phylogenet. Evol. 2009, 50, 423–436. [Google Scholar] [CrossRef]
  23. Crease, T.J.; Omilian, A.R.; Costanzo, K.S.; Taylor, D.J. Transcontinental phylogeography of the Daphnia pulex species complex. PLoS ONE 2012, 7, e46620. [Google Scholar] [CrossRef] [Green Version]
  24. Fields, P.D.; Obbard, D.J.; McTaggart, S.J.; Galimov, Y.; Little, T.J.; Ebert, D. Mitogenome phylogeographic analysis of a planktonic crustacean. Mol. Phylogenet. Evol. 2018, 129, 138–148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Taylor, D.J.; Connelly, S.J.; Kotov, A.A. The Intercontinental phylogeography of neustonic daphniids. Sci. Rep. 2020, 10, 1818. [Google Scholar] [CrossRef] [PubMed]
  26. Petrusek, A.; Hobaek, A.; Nilssen, J.P.; Skage, M.; Cerny, M.; Brede, N.; Schwenk, K. A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda). Zool. Scr. 2008, 37, 507–519. [Google Scholar] [CrossRef]
  27. Zuykova, E.I.; Bochkarev, N.A.; Taylor, D.J.; Kotov, A.A. Unexpected endemism in the Daphnia longispina complex (Crustacea: Cladocera) in Southern Siberia. PLoS ONE 2019, 14, e0221527. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Benzie, J.A.H. The Genus Daphnia (Including Daphniopsis): Anomopoda: Daphniidae; Kenobi Productions: Ghent, Belgium, 2005; ISBN 9057821516. [Google Scholar]
  29. Kotov, A.A. A critical review of the current taxonomy of the genus Daphnia O. F. Müller, 1785 (Anomopoda, Cladocera). Zootaxa 2015, 3911, 184–200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Shaw, J.R.; Pfrender, M.E.; Eads, B.D.; Klaper, R.; Callaghan, A.; Sibly, R.M.; Colson, I.; Jansen, B.; Gilbert, D.; Colbourne, J.K. Daphnia as an emerging model for toxicological genomics. In Comparative Toxicogenomics; Hogstrand, C., Kille, P., Eds.; Elsevier: Amsterdam, The Netherlands; London, UK, 2008; pp. 165–328. ISBN 9780444532749. [Google Scholar]
  31. Tkaczyk, A.; Bownik, A.; Dudka, J.; Kowal, K.; Slaska, B. Daphnia magna model in the toxicity assessment of pharmaceuticals: A review. Sci. Total Environ. 2021, 763, 143038. [Google Scholar] [CrossRef]
  32. Fields, P.D.; Reisser, C.; Dukić, M.; Haag, C.R.; Ebert, D. Genes mirror geography in Daphnia magna. Mol. Ecol. 2015, 24, 4521–4536. [Google Scholar] [CrossRef]
  33. Bekker, E.I.; Karabanov, D.P.; Galimov, Y.R.; Haag, C.R.; Neretina, T.V.; Kotov, A.A. Phylogeography of Daphnia magna Straus (Crustacea: Cladocera) in Northern Eurasia: Evidence for a deep longitudinal split between mitochondrial lineages. PLoS ONE 2018, 13, e0194045. [Google Scholar] [CrossRef] [PubMed]
  34. Kotov, A.A.; Karabanov, D.P.; Bekker, E.I.; Neretina, T.V.; Taylor, D.J. Phylogeography of the Chydorus sphaericus Group (Cladocera: Chydoridae) in the Northern Palearctic. PLoS ONE 2016, 11, e0168711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Fernando, C.H.; Paggi, J.C.; Rajapaksa, R. Daphnia in tropical lowlands. In Daphnia. Memorie Dell’ Istituto Italiano di Ldrobiologia; Peters, R.H., De Bernardi, R., Eds.; Istituto Italiano di Idrobiologia: Pallanza, Italy, 1987; Volume 45, pp. 107–141. [Google Scholar]
  36. Kotov, A.A.; Taylor, D.J. Mesozoic fossils (145 Mya) suggest the antiquity of the subgenera of Daphnia and their coevolution with chaoborid predators. BMC Evol. Biol. 2011, 11, 129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Karabanov, D.P.; Garibian, P.G.; Bekker, E.I.; Sabitova, R.Z.; Kotov, A.A. Genetic signature of a past anthropogenic transportation of a Far-Eastern endemic Cladoceran (Crustacea: Daphniidae) to the Volga Basin. Water 2021, 13, 2589. [Google Scholar] [CrossRef]
  38. Alonso, M. Crustacea, Branchiopoda: Fauna Iberica; Museo Nacional de Ciencias Naturales: Madrid, Spain, 1996; Volume 7, ISBN 9788400075712. [Google Scholar]
  39. Petrusek, A.; Tollrian, R.; Schwenk, K.; Haas, A.; Laforsch, C. A “crown of thorns” is an inducible defense that protects Daphnia against an ancient predator. Proc. Natl. Acad. Sci. USA 2009, 106, 2248–2252. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Popova, E.V.; Petrusek, A.; Kořínek, V.; Mergeay, J.; Bekker, E.I.; Karabanov, D.P.; Galimov, Y.R.; Neretina, T.V.; Taylor, D.J.; Kotov, A.A. Revision of the Old World Daphnia (Ctenodaphnia) similis group (Cladocera: Daphniidae). Zootaxa 2016, 4161, 1–40. [Google Scholar] [CrossRef] [PubMed]
  41. Hamza, W.; Ramadan, G.; AlKaabi, M. Morphological and molecular identification of first recorded Cladoceran organisms in the desert of Abu Dhabi, UAE. MOJ Eco. Environ. Sci. 2018, 3, 220–224. [Google Scholar] [CrossRef] [Green Version]
  42. Kotov, A.A. Morphology and Phylogeny of the Anomopoda (Crustacea: Cladocera); KMK Scientific Press Ltd.: Moscow, Russia, 2013; ISBN 9785873179237. [Google Scholar]
  43. Okonechnikov, K.; Golosova, O.; Fursov, M. Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics 2012, 28, 1166–1167. [Google Scholar] [CrossRef] [Green Version]
  44. Sayers, E.W.; Beck, J.; Brister, J.R.; Bolton, E.E.; Canese, K.; Comeau, D.C.; Funk, K.; Ketter, A.; Kim, S.; Kimchi, A.; et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2020, 48, D9–D16. [Google Scholar] [CrossRef] [Green Version]
  45. Katoh, K.; Rozewicki, J.; Yamada, K.D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019, 20, 1160–1166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Trifinopoulos, J.; Nguyen, L.-T.; von Haeseler, A.; Minh, B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016, 44, W232–W235. [Google Scholar] [CrossRef] [Green Version]
  48. Posada, D.; Buckley, T.R. Model selection and model averaging in phylogenetics: Advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 2004, 53, 793–808. [Google Scholar] [CrossRef] [PubMed]
  49. Vaidya, G.; Lohman, D.J.; Meier, R. SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 2011, 27, 171–180. [Google Scholar] [CrossRef]
  50. Nguyen, L.-T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
  51. Minh, B.Q.; Nguyen, M.A.T.; Haeseler, A. von. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 2013, 30, 1188–1195. [Google Scholar] [CrossRef]
  52. Guindon, S.; Dufayard, J.-F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59, 307–321. [Google Scholar] [CrossRef] [Green Version]
  53. Heled, J.; Drummond, A.J. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 2010, 27, 570–580. [Google Scholar] [CrossRef] [Green Version]
  54. Bouckaert, R.; Vaughan, T.G.; Barido-Sottani, J.; Duchene, S.; Fourment, M.; Gavryushkina, A.; Heled, J.; Jones, G.; Kuhnert, D.; de Maio, N.; et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 2019, 15, e1006650. [Google Scholar] [CrossRef] [Green Version]
  55. Drummond, A.J.; Suchard, M.A.; Xie, D.; Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29, 1969–1973. [Google Scholar] [CrossRef] [Green Version]
  56. Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G.; Suchard, M.A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018, 67, 901–904. [Google Scholar] [CrossRef] [Green Version]
  57. Drummond, A.J.; Bouckaert, R.R. Bayesian Evolutionary Analysis with BEAST2; Cambridge University Press: Cambridge, UK, 2015; ISBN 978-1-107-01965-2. [Google Scholar]
  58. Hipsley, C.A.; Muller, J. Beyond fossil calibrations: Realities of molecular clock practices in evolutionary biology. Front. Genet. 2014, 5, 138. [Google Scholar] [CrossRef]
  59. Cornetti, L.; Fields, P.D.; Van Damme, K.; Ebert, D. A fossil-calibrated phylogenomic analysis of Daphnia and the Daphniidae. Mol. Phylogenet. Evol. 2019, 137, 250–262. [Google Scholar] [CrossRef]
  60. Douglas, J.; Zhang, R.; Bouckaert, R. Adaptive dating and fast proposals: Revisiting the phylogenetic relaxed clock model. PLoS Comput. Biol. 2021, 17, e1008322. [Google Scholar] [CrossRef] [PubMed]
  61. Gernhard, T. The conditioned reconstructed process. J. Theor. Biol. 2008, 253, 769–778. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Barido-Sottani, J.; Boskova, V.; Du Plessis, L.; Kuhnert, D.; Magnus, C.; Mitov, V.; Muller, N.F.; PecErska, J.; Rasmussen, D.A.; Zhang, C.; et al. Taming the BEAST—A community teaching material resource for BEAST2. Syst. Biol. 2018, 67, 170–174. [Google Scholar] [CrossRef] [PubMed]
  63. Leigh, J.W.; Bryant, D.; Nakagawa, S. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 2015, 6, 1110–1116. [Google Scholar] [CrossRef]
  64. Jones, G. Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J. Math. Biol. 2017, 74, 447–467. [Google Scholar] [CrossRef] [PubMed]
  65. Vitecek, S.; Kucinic, M.; Previsic, A.; Zivic, I.; Stojanovic, K.; Keresztes, L.; Balint, M.; Hoppeler, F.; Waringer, J.; Graf, W.; et al. Integrative taxonomy by molecular species delimitation: Multi-locus data corroborate a new species of Balkan Drusinae micro-endemics. BMC Evol. Biol. 2017, 17, 129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
  67. Collins, R.A.; Boykin, L.M.; Cruickshank, R.H.; Armstrong, K.F. Barcoding’s next top model: An evaluation of nucleotide substitution models for specimen identification. Methods Ecol. Evol. 2012, 3, 457–465. [Google Scholar] [CrossRef]
  68. Nei, M.; Kumar, S. Molecular Evolution and Phylogenetics; Oxford University Press: New York, NY, USA, 2000; ISBN 0195135857. [Google Scholar]
  69. Hudec, I. A comparison of populations from the Daphnia similis group (Cladocera: Daphniidae). Hydrobiologia 1991, 225, 9–22. [Google Scholar] [CrossRef]
  70. Hebert, P.D.N.; Stoeckle, M.Y.; Zemlak, T.S.; Francis, C.M. Identification of Birds through DNA Barcodes. PLoS Biol. 2004, 2, e312. [Google Scholar] [CrossRef] [Green Version]
  71. Xiang, X.-F.; Ji, G.-H.; Chen, S.-Z.; Yu, G.-L.; Xu, L.; Han, B.-P.; Kotov, A.A.; Dumont, H.J. Annotated Checklist of Chinese Cladocera (Crustacea: Branchiopoda). Part I. Haplopoda, Ctenopoda, Onychopoda and Anomopoda (families Daphniidae, Moinidae, Bosminidae, Ilyocryptidae). Zootaxa 2015, 3904, 1–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Zharov, A.A.; Neretina, A.N.; Rogers, D.C.; Reshetova, S.A.; Sinitsa, S.M.; Kotov, A.A. Pleistocene Branchiopods (Cladocera, Anostraca) from Transbaikalian Siberia demonstrate morphological and ecological stasis. Water 2020, 12, 3063. [Google Scholar] [CrossRef]
  73. Grandcolas, P.; Nattier, R.; Trewick, S. Relict species: A relict concept? Trends Ecol. Evol. 2014, 29, 655–663. [Google Scholar] [CrossRef]
  74. Petrusek, A. The population of the Daphnia similis species complex in Germany after 110 years—A new case of species introduction? Senckenb. Biol. 2003, 82, 11–14. [Google Scholar]
  75. Korovchinsky, N.M. The Cladocera (Crustacea: Branchiopoda) as a relict group. Zool. J. Linn. Soc. 2006, 147, 109–124. [Google Scholar] [CrossRef] [Green Version]
  76. Dumont, H.J. Relict Distribution Patterns of Aquatic Animals: Another Tool in Evaluating Late Pleistocene Climate Changes in the Sahara and Sahel. In Palaeoecology of Africa and the Surrounding Islands, 1st ed.; Routledge: Abingdon-on-Thames, UK, 1982; Volume 14, ISBN 9780203744529. [Google Scholar]
  77. Kehl, M. Quaternary climate change in Iran—The state of knowledge. Erdkunde 2009, 63, 1–17. [Google Scholar] [CrossRef]
  78. Parker, A.G. Pleistocene climate change in Arabia: Developing a framework for Hominin dispersal over the last 350 ka. In The Evolution of Human Populations in Arabia. Vertebrate Paleobiology and Paleoanthropology; Petraglia, M.D., Rose, J.I., Eds.; Springer: Dordrecht, The Netherlands, 2010; pp. 39–49. ISBN 978-90-481-2718-4. [Google Scholar]
  79. Petraglia, M.D.; Parton, A.; Groucutt, H.S.; Alsharekh, A. Green Arabia: Human prehistory at the crossroads of continents. Quat. Int. 2015, 382, 1–7. [Google Scholar] [CrossRef] [Green Version]
  80. Ma, X.; Ni, Y.; Wang, X.; Hu, W.; Yin, M. Clonal diversity and substantial genetic divergence of the Daphnia similis species complex in Chinese lakes: Possible adaptations to the uplift of the Qinghai—Tibetan Plateau. Limnol. Oceanogr. 2019, 64, 2725–2737. [Google Scholar] [CrossRef]
  81. Ma, X.; Ni, Y.; Wang, X.; Hu, W.; Yin, M. Lineage diversity, morphological and genetic divergence in Daphnia magna (Crustacea) among Chinese lakes at different altitudes. Contrib. Zool. 2020, 89, 450–470. [Google Scholar] [CrossRef]
  82. Bekker, E.I.; Karabanov, D.P.; Galimov, Y.R.; Kotov, A.A. DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera). PLoS ONE 2016, 11, e0161737. [Google Scholar] [CrossRef] [Green Version]
  83. Zuykova, E.I.; Simonov, E.P.; Bochkarev, N.A.; Abramov, S.A.; Sheveleva, N.G.; Kotov, A.A. Contrasting phylogeographic patterns and demographic history in closely related species of Daphnia longispina group (Crustacea: Cladocera) with focus on North-Eastern Eurasia. PLoS ONE 2018, 13, e0207347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Havel, J.E.; Colbourne, J.K.; Hebert, P.D.N. Reconstructing the history of intercontinental dispersal in Daphnia lumholtzi by use of genetic markers. Limnol. Oceanogr. 2000, 45, 1414–1419. [Google Scholar] [CrossRef]
  85. Karabanov, D.P.; Bekker, E.I.; Kotov, A.A. Underestimated consequences of biological invasions in phylogeographic reconstructions as seen in Daphnia magna (Crustacea, Cladocera). Zool. Zh. 2020, 99, 1232–1241. [Google Scholar] [CrossRef]
  86. Kotov, A.A.; Garibian, P.G.; Neretina, A.N.; Marrone, F. A redescription of the Mediterranean endemic cladoceran Daphnia chevreuxi Richard, 1896 (Cladocera: Daphniidae). Zootaxa 2022, 5125, 205–228. [Google Scholar] [CrossRef]
  87. Timmermann, A.; Friedrich, T. Late Pleistocene climate drivers of early human migration. Nature 2016, 538, 92–95. [Google Scholar] [CrossRef] [PubMed]
  88. Bae, C.J.; Douka, K.; Petraglia, M.D. On the origin of modern humans: Asian perspectives. Science 2017, 358, eaai9067. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Figure 1. Daphnia arabica sp. nov., parthenogenetic females from Al Shuwaib Dam, near Al Ain city, United Arab Emirates, paratypes. (a) An adult female, lateral view. (b) A female of smaller size, lateral view. (c) Head. (d) Labrum. (e) Valve and its armature. (f) Armature of valve on higher magnification, inner view. (g) Armature of posterior portion of valve, inner view. (h) Armature of ventral portion of valve, inner view. (i), Rostrum and antenna I. All scale bars are 0.1 mm.
Figure 1. Daphnia arabica sp. nov., parthenogenetic females from Al Shuwaib Dam, near Al Ain city, United Arab Emirates, paratypes. (a) An adult female, lateral view. (b) A female of smaller size, lateral view. (c) Head. (d) Labrum. (e) Valve and its armature. (f) Armature of valve on higher magnification, inner view. (g) Armature of posterior portion of valve, inner view. (h) Armature of ventral portion of valve, inner view. (i), Rostrum and antenna I. All scale bars are 0.1 mm.
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Figure 2. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Postabdomen. (b) Distal portion of postabdomen. (c) Antenna II. (d) Thoracic limb I. (e) Distal portion of thoracic limb I. All scale bars are 0.1 mm.
Figure 2. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Postabdomen. (b) Distal portion of postabdomen. (c) Antenna II. (d) Thoracic limb I. (e) Distal portion of thoracic limb I. All scale bars are 0.1 mm.
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Figure 3. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a,b) Postabdomen. (ce) Postabdominal claws. Scale bars are 0.2 mm for (a,b); 0.1 mm for (d), 0.02 mm for (c,e).
Figure 3. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a,b) Postabdomen. (ce) Postabdominal claws. Scale bars are 0.2 mm for (a,b); 0.1 mm for (d), 0.02 mm for (c,e).
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Figure 4. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Thoracic limb II. (b,c) Fragments of thoracic limb II on higher magnification. (d) Thoracic limb III. (e) Gnathobase of thoracic limb III. All scale bars are 0.1 mm.
Figure 4. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Thoracic limb II. (b,c) Fragments of thoracic limb II on higher magnification. (d) Thoracic limb III. (e) Gnathobase of thoracic limb III. All scale bars are 0.1 mm.
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Figure 5. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Thoracic limb IV. (b) Fragment of gnathobase of thoracic limb IV. (c) Thoracic limb V. (d,e) Distal portion of thoracic limb V. All scale bars are 0.1 mm.
Figure 5. Daphnia arabica sp. nov., a parthenogenetic female from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Thoracic limb IV. (b) Fragment of gnathobase of thoracic limb IV. (c) Thoracic limb V. (d,e) Distal portion of thoracic limb V. All scale bars are 0.1 mm.
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Figure 6. Daphnia arabica sp. nov., an ephippial female (ac) and adult male (dh) from Al Shuwaib Dam, near Al Ain city, United Arab Emirates, paratypes. (a) Ephippial female, lateral view. (b) Ephippium, lateral view. (c) Ornamentation of ephippium under higher magnification. (d) Male, lateral view. (e) Head. (f) Labrum. (g) Valve. (h) Postabdomen. All scale bars are 0.1 mm.
Figure 6. Daphnia arabica sp. nov., an ephippial female (ac) and adult male (dh) from Al Shuwaib Dam, near Al Ain city, United Arab Emirates, paratypes. (a) Ephippial female, lateral view. (b) Ephippium, lateral view. (c) Ornamentation of ephippium under higher magnification. (d) Male, lateral view. (e) Head. (f) Labrum. (g) Valve. (h) Postabdomen. All scale bars are 0.1 mm.
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Figure 7. Daphnia arabica sp. nov., ephippial females from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a,b) Ephippium, lateral view. (c,d) Central portion of ephippium with resting eggs. (e) Anterior portion of ephippium, lateral view. (f) Central portion of ephippium dorsal margin. (g) Posterior portion of ephippium. (h) Central portion of ephippium on higher magnification. (i) Ephippium, dorsal view. (j) Anterior portion of ephippium, dorsal view. (k,l) Ephippium dorsal margin on different magnifications. Scale bars are 0.5 mm for (a,b); 0.1 mm for (ce,j,k); 0.05 mm for (f,g); 0.02 mm for (h,l).
Figure 7. Daphnia arabica sp. nov., ephippial females from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a,b) Ephippium, lateral view. (c,d) Central portion of ephippium with resting eggs. (e) Anterior portion of ephippium, lateral view. (f) Central portion of ephippium dorsal margin. (g) Posterior portion of ephippium. (h) Central portion of ephippium on higher magnification. (i) Ephippium, dorsal view. (j) Anterior portion of ephippium, dorsal view. (k,l) Ephippium dorsal margin on different magnifications. Scale bars are 0.5 mm for (a,b); 0.1 mm for (ce,j,k); 0.05 mm for (f,g); 0.02 mm for (h,l).
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Figure 8. Daphnia arabica sp. nov., an ephippial female (af) and a dumped ephippium (gi) from Al Shuwaib Dam, near Al Ain city, United Arab Emirates (material from the laboratory culture). (a) Ephippial female, lateral view. (b) Head. (c) Rostrum. (d) Ephippium. (e) Ephippium with resting eggs. (f) Ornamentation of central portion of ephippium on higher magnification. (g) Dumped ephippium. (h) Ephippium with resting eggs. (i) Ornamentation of central portion of ephippium. Scale bars are 0.5 mm for (a); 0.2 mm for (b,d,g); 0.1 mm for (e,h); 0.02 mm for (c,f,i).
Figure 8. Daphnia arabica sp. nov., an ephippial female (af) and a dumped ephippium (gi) from Al Shuwaib Dam, near Al Ain city, United Arab Emirates (material from the laboratory culture). (a) Ephippial female, lateral view. (b) Head. (c) Rostrum. (d) Ephippium. (e) Ephippium with resting eggs. (f) Ornamentation of central portion of ephippium on higher magnification. (g) Dumped ephippium. (h) Ephippium with resting eggs. (i) Ornamentation of central portion of ephippium. Scale bars are 0.5 mm for (a); 0.2 mm for (b,d,g); 0.1 mm for (e,h); 0.02 mm for (c,f,i).
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Figure 9. Daphnia arabica sp. nov., an adult male from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Male, lateral view. (b,c) Head. (d) Postabdomen. (e,f) Postabdominal claws. (g,h) Antenna I. (i) Antenna II. Scale bars are 1 mm for (a); 0.2 mm for (b); 0.1 mm for (c,d,i); 0.05 mm for (e,g); 0.02 mm for (f,h).
Figure 9. Daphnia arabica sp. nov., an adult male from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Male, lateral view. (b,c) Head. (d) Postabdomen. (e,f) Postabdominal claws. (g,h) Antenna I. (i) Antenna II. Scale bars are 1 mm for (a); 0.2 mm for (b); 0.1 mm for (c,d,i); 0.05 mm for (e,g); 0.02 mm for (f,h).
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Figure 10. Daphnia arabica sp. nov., an adult male from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Postabdomen. (b) Antenna I. (c,d) Distal portions of antenna I. (e) Thoracic limb I. (f,g) Fragments of thoracic limb I on higher magnification. (h) Fragment of thoracic limb II on higher magnification. (i) Thoracic limb V. All scale bars are 0.1 mm.
Figure 10. Daphnia arabica sp. nov., an adult male from Al Shuwaib Dam, near Al Ain city, United Arab Emirates. (a) Postabdomen. (b) Antenna I. (c,d) Distal portions of antenna I. (e) Thoracic limb I. (f,g) Fragments of thoracic limb I on higher magnification. (h) Fragment of thoracic limb II on higher magnification. (i) Thoracic limb V. All scale bars are 0.1 mm.
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Figure 11. Limb V in D. (C.) sinensis group. (a,b) Thoracic limb V of adult female of Daphnia inopinata Popova et al., 2016 from Munchen Siger, Germany (type locality); (c) Thoracic limb V of adult female of Daphnia similoides Hudec, 1991 from Ooty Lake in Nilgiris Mountains, Tamil Nadu, India (type locality). All scale bars are 0.1 mm.
Figure 11. Limb V in D. (C.) sinensis group. (a,b) Thoracic limb V of adult female of Daphnia inopinata Popova et al., 2016 from Munchen Siger, Germany (type locality); (c) Thoracic limb V of adult female of Daphnia similoides Hudec, 1991 from Ooty Lake in Nilgiris Mountains, Tamil Nadu, India (type locality). All scale bars are 0.1 mm.
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Figure 12. Phylogenetic ultrametric tree based on three mitochondrial genes (12S, 16S, COI) for Daphnia (Ctenodaphnia) with relaxed molecular clock estimates based on fossil calibration points. The bars depict the 95% highest probability density (HPD) interval of the estimated divergence times. Prior probability of branches is coded by the colour gradient from red (low) to green (high). Node supports for key points are: UFboot (ML) for the first digit/value of the SH-aLRT test for the second digits. Results of the STACEY delimitation are represented by bars of different colours on the right side: blue—now inhabit mainly the “Laurasian“ territories, red—mainly inhabit “Gondwanan“ territories and closest to the former ones (only aborigenous range, not taking into consideration recent anthropogenic invasions), purple—distributed through both territories, white with blue frame—invader of unknown origin.
Figure 12. Phylogenetic ultrametric tree based on three mitochondrial genes (12S, 16S, COI) for Daphnia (Ctenodaphnia) with relaxed molecular clock estimates based on fossil calibration points. The bars depict the 95% highest probability density (HPD) interval of the estimated divergence times. Prior probability of branches is coded by the colour gradient from red (low) to green (high). Node supports for key points are: UFboot (ML) for the first digit/value of the SH-aLRT test for the second digits. Results of the STACEY delimitation are represented by bars of different colours on the right side: blue—now inhabit mainly the “Laurasian“ territories, red—mainly inhabit “Gondwanan“ territories and closest to the former ones (only aborigenous range, not taking into consideration recent anthropogenic invasions), purple—distributed through both territories, white with blue frame—invader of unknown origin.
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Figure 13. A median-joining networks of studied taxa based on short 12S fragments.
Figure 13. A median-joining networks of studied taxa based on short 12S fragments.
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Table 1. Estimates of evolutionary divergence over sequence pairs between major clades of Daphnia using COI gene sequences. The number of base differences per site as averaged over all sequence pairs between the groups are shown below the diagonal. The number of base differences per site as averaged over all sequence pairs within each group are shown in the diagonal. Standard error (in bootstrap 100 replicates) estimates are shown above the diagonal. Codon positions included were 1st + 2nd + 3rd (487 positions in the final dataset). Groups: ar—arabica; at—atkinsoni; br—barbata; ca—carinata; ce—cephalata; ex—exilis; in—inopinata; lc—longicephalata; ls—longispina; lz—lumholtzi; mg—magna; nv—nivalis; pu—pulex; sl—salinifera; sm—similis; sn—sinensis; sp—spinulata.
Table 1. Estimates of evolutionary divergence over sequence pairs between major clades of Daphnia using COI gene sequences. The number of base differences per site as averaged over all sequence pairs between the groups are shown below the diagonal. The number of base differences per site as averaged over all sequence pairs within each group are shown in the diagonal. Standard error (in bootstrap 100 replicates) estimates are shown above the diagonal. Codon positions included were 1st + 2nd + 3rd (487 positions in the final dataset). Groups: ar—arabica; at—atkinsoni; br—barbata; ca—carinata; ce—cephalata; ex—exilis; in—inopinata; lc—longicephalata; ls—longispina; lz—lumholtzi; mg—magna; nv—nivalis; pu—pulex; sl—salinifera; sm—similis; sn—sinensis; sp—spinulata.
Aratbrcaceexinlclslzmgnvpuslsmsnsp
ar-1.91.71.81.31.61.41.52.11.51.31.81.61.91.51.21.7
at17.80.21.51.71.62.11.71.61.91.61.51.72.01.91.51.52.0
br19.019.70.51.51.51.71.51.42.11.41.71.62.31.71.61.61.6
ca17.719.016.0-1.61.61.31.32.11.51.71.81.91.81.41.51.6
ce16.215.915.913.3-1.71.31.32.11.21.51.81.71.61.21.51.7
ex19.121.021.118.721.1-1.81.81.51.61.52.11.81.81.81.80.8
in11.117.816.416.015.018.7-1.61.91.31.51.71.71.61.41.11.8
lc15.217.616.912.913.619.316.2-2.31.31.61.71.91.81.61.51.8
ls22.420.422.720.122.420.323.020.90.12.01.92.02.11.92.01.91.5
lz15.716.818.413.714.520.315.516.122.60.41.51.71.91.71.21.21.5
mg14.218.318.516.817.716.915.117.221.116.30.91.72.11.61.31.61.6
nv17.918.818.413.816.219.916.813.321.816.918.3-2.21.51.71.82.0
pu23.423.322.518.920.722.022.623.222.622.623.121.40.42.11.81.71.9
sl18.717.418.513.115.217.915.817.521.416.017.214.223.4-1.51.81.9
sm14.918.216.715.915.219.313.715.522.016.714.516.822.016.80.71.51.9
sn9.716.316.016.114.617.08.414.721.715.015.017.621.516.314.00.21.7
sp19.920.220.918.920.33.719.118.121.119.417.418.923.217.719.916.9-
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Hamza, W.; Neretina, A.N.; Al Neyadi, S.E.S.; Amiri, K.M.A.; Karabanov, D.P.; Kotov, A.A. Discovery of a New Species of Daphnia (Crustacea: Cladocera) from the Arabian Peninsula Revealed a Southern Origin of a Common Northern Eurasian Species Group. Water 2022, 14, 2350. https://doi.org/10.3390/w14152350

AMA Style

Hamza W, Neretina AN, Al Neyadi SES, Amiri KMA, Karabanov DP, Kotov AA. Discovery of a New Species of Daphnia (Crustacea: Cladocera) from the Arabian Peninsula Revealed a Southern Origin of a Common Northern Eurasian Species Group. Water. 2022; 14(15):2350. https://doi.org/10.3390/w14152350

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Hamza, Waleed, Anna N. Neretina, Shamma Eisa Salem Al Neyadi, Khaled M.A. Amiri, Dmitry P. Karabanov, and Alexey A. Kotov. 2022. "Discovery of a New Species of Daphnia (Crustacea: Cladocera) from the Arabian Peninsula Revealed a Southern Origin of a Common Northern Eurasian Species Group" Water 14, no. 15: 2350. https://doi.org/10.3390/w14152350

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