, Volume 801, Issue 1, pp 21–32 | Cite as

Molecular and morphological data suggest weak phylogeographic structure in the fairy shrimp Streptocephalus torvicornis (Branchiopoda, Anostraca)

  • Ilias Kappas
  • Graziella Mura
  • Dimitra Synefiaridou
  • Federico Marrone
  • Giuseppe Alfonso
  • Miguel Alonso
  • Theodore J. Abatzopoulos


Inland aquatic organisms almost ubiquitously display a pattern of marked provincialism characterized by substantial population differentiation and genealogical discontinuities. This is the result of strong priority effects and local adaptation following dispersal and colonization of new habitats. We present a case that defies this biogeographic paradigm. We have investigated the phylogeography of the fairy shrimp Streptocephalus torvicornis across its circum-Mediterranean and Eurasian distribution. Based on three independent datasets, namely sequence variation at 12S and 16S rRNA, cyst morphology and male second antenna characters, we discern a pattern of extensive genetic and morphological homogeneity pointing to unhindered gene flow and widespread connectivity among populations. These intriguing findings may provisionally be explained by (i) a high dispersal frequency overwhelming the ability of a population to maintain resource monopolization, (ii) an outbreeding vigour opportunity offered to secondary immigrants, (iii) an ecological equivalence of genotypes generating long-term immigration–extinction equilibria and buffering genetic diversity over spatial scales, (iv) enhanced bird-mediated dispersal in open habitats as opposed to ponds surrounded by forests or shrub, or (v) a shallow population history with little time for substantial genetic differentiation.


Population structure Mitochondrial DNA Genetic differentiation Inland waters Cyst morphology Male antenna 


Research on inland aquatic organisms has been highly influential in putting together integrative hypotheses on historical biogeography, phylogeography and ecology. Over the past twenty years or so, significant progress in those fields has been achieved using continental zooplankters as study systems. As a result, the early apparent interdisciplinary chasms (Wiens & Donoghue, 2004) have now been adequately bridged by new research theories and tools that run the full distance of relevant questions (from population structure and cryptic speciation to dispersal and extinction) at different taxonomic depths.

Organisms inhabiting the terrestrial aquatic realm are excellent models for the study of changes at both ecological and evolutionary scales (Hairston et al., 2005). Conducive to such research are their distinctive biology and the physical structure of their environments. Typical inland waters comprise vernal pools, seasonal ponds, wetlands, playas, salt lakes and others. They resemble “islands on a terrestrial sea”, varying considerably in space, time, isolation and water chemistry (Rogers, 2015). By nature, these settings pose an insurmountable obstacle to dispersal given the delicate and fragile body structure of inland zooplankton. Yet, through a remarkable adaptation, the production of dehydrated diapausing propagules (also called resting stages), continental zooplankters are able to passively disperse and colonize new habitats over various scales either via wind or animal vectors (Figuerola & Green, 2002; Vanschoenwinkel et al., 2008). A large body of evidence consistently supports the extremely high potential for passive dispersal, typically exemplified by cases of fast colonization of newly formed water bodies or, on a greater scale, by the rapid post-glacial recolonization of northern regions (see Incagnone et al., 2015 and references therein).

The above considerations sparked the idea that aquatic taxa capable of producing resting stages would show a cosmopolitan distribution, limited only by the ecological characteristics of the available habitats. Coined as “Everything is Everywhere” (EiE) (see also Williams, 2011), this hypothesis also made specific predictions regarding the genetic architecture of the relevant taxa. It was thus envisaged that the absence of effective barriers to gene flow would translate to a signature of genetic homogeneity, registered as a lack of substantial population structure and differentiation among populations and, phenotypically, as a striking morphological uniformity. Possibly undisputed patterns, consistent with those predictions, have so far been documented by only a handful of studies (e.g. Finlay, 2002; Zofkova & Timms, 2009; Aguilar, 2011; Schwentner et al., 2012; Audet et al., 2013). On the contrary, a pile of evidence has been gathered showing marked phylogeographic structure in inland water organisms (see De Meester et al., 2002; Incagnone et al., 2015). Consequently, there has been a shift towards “provincialism”, as opposed to “cosmopolitanism”, as the default biogeographic hypothesis for aquatic invertebrates. In a genealogical context, sharply demarcated phylogroups, cryptic species complexes and allopatric divergence are now the working scenarios encompassing the continuum from gene splitting to population differentiation and speciation (see Maniatsi et al., 2009 and references therein). The new premise, known as the “Monopolization Hypothesis” (De Meester et al., 2002), was inspired by a high dispersal—low gene flow paradox implicit in empirical genetic data. This hypothesis interpreted observed patterns as a reflection of historical colonization events due to priority effects and strong local adaptation.

On this basis, we have made a first effort to investigate the phylogeography of the freshwater fairy shrimp Streptocephalus torvicornis Waga, 1842. Molecular data on the anostracan monotypic family Streptocephalidae are rather fragmentary. Streptocephalids feature in studies focusing either on the ordinal relationships within Branchiopoda (de Waard et al., 2006) or the familial relationships within Anostraca (Remigio & Hebert, 2000; Weekers et al., 2002). The only study focused explicitly on Streptocephalus is that by Daniels et al. (2004), yet this too probes the phylogenetic relationships of the different species. Therefore, information on levels of intraspecific diversity and patterns of population differentiation in this speciose genus are generally lacking. Streptocephalus torvicornis shows a wide distribution, occurring in Northern Africa, Europe and Asia (Dumont et al., 1991, 1995; Mura & Cottarelli, 1998). From a molecular perspective, the species is virtually unstudied (only three GenBank sequences exist; COI, 12S, 18S) and the only piece of information regarding its biogeography comes from the study of Dumont et al. (1995). Using occurrence data and scanning electron microscopy of male antennae characters, these authors identified a distributional pattern (“pincers-like”, see Dumont et al., 1995) with two obvious hiatuses. In the west, Streptocephalus torvicornis occurs in the Maghreb and Spain (up to the Pyrenees barrier) and in the east it is found in the Middle East and Balkan Peninsula up to the Pannonian plain. The first hiatus runs along the Nile Valley and the Horn of Africa while the second one extends from the Benelux countries and France down the entire Peninsular Italy with the notable exception of Apulia (Alfonso, 2017). According to Dumont et al. (1995), the first hiatus is probably related to the presence of introgressed populations with the closely related species S. rubricaudatus. The second hiatus has been attributed to the effects of the Würm III glaciation on European populations.

In this work, we have used novel sequence data from two mitochondrial DNA regions, 12S and 16S, together with patterns of cyst morphology and male second antenna from populations of S. torvicornis across its range in order to examine the patterns of geographic partitioning and levels of intraspecific variability. Initially, we made efforts to acquire sequence data from another two mitochondrial loci, Cytb and COI, which are more diverse and informative than the rRNA regions and are typically used in phylogeographic assays. However, the obtained sequence chromatograms were of low quality and, therefore, these two loci were subsequently dropped from the study. Despite the lower information content of 12S and 16S rRNA, these mitochondrial markers are still useful in evaluating hypotheses at various taxonomic levels (Richter et al., 2007; Ketmaier et al., 2012; Pinceel et al., 2013a, b; Ladoukakis & Zouros, 2017) and seem to be less prone to pseudogene co-amplification (Buhay, 2009; Thum & Harrison, 2009; Baeza & Fuentes, 2013; Marrone et al., 2013). The morphological characters, cyst surface ornamentation and male second antenna, are commonly used as established phenotypic variables in the Streptocephalus literature (and also anostracans in general) dealing with inter- and intrapopulation differences (see Thiéry, 1987; Dumont et al., 1991, 1995; Maeda-Martinez et al., 1995a, b; Mura & Rossetti, 2010; Bruner et al., 2013; Gandolfi et al., 2015).

Contrary to expectations and in clear antithesis to the marked phylogeographic structuring seen in the vast majority of inland zooplankters, we identify extensive genetic as well as morphological homogeneity pointing to unhindered gene flow and widespread connectivity.

Materials and methods

Dataset assembly

We sampled 24 populations of S. torvicornis (Table 1) covering most of its distribution in Europe (Spain, Italy, Romania, FYROM, Serbia, Slovakia, Ukraine, European Russia), Northern Africa (Morocco, Tunisia) and Asia (Asian Russia, Georgia, Iran). Three independent datasets were assembled. In the first dataset, 54 individuals from 15 populations were screened for sequence variation at two mitochondrial DNA regions. In the second dataset, cyst surface ornamentation was assayed in 21 populations. In the third dataset, 54 males from 15 populations were analysed for morphological characters of the second antenna.
Table 1

Populations of Streptocephalus torvicornis analysed. Numbers in subscript of the second column refer to individuals used in phylogenetic analyses


Site code individual

Collection date

Crimea, Tauritcheskaja, Gussevka2

04/03/2005* (code: 9611)

FYROM, Loznani1


GEORGIA, Tbilisi, Lake Kukijskoe2/3

−/−/1960* (code: 42/53806)

IRAN, Qum Tappeh1/2/3



ITALY, Apulia, San Donaci1/2/3



ITALY, Apulia, Conversano1/2/3



ITALY, Apulia, Tremiti Archipelago, San Nicola Island1/2/3



ITALY, Apulia, Tremiti Archipelago, San Nicola Island3



MOROCCO, Mamora1/2



ROMANIA, Ariuşd1/2


RUSSIA, Krasnodar2/3

13/08/1915* (code: 15336)

RUSSIA, Saratov, Volga River Biological Station2/3

−/−/1900* (code: 135-903/13)

RUSSIA, Kjahta, Transbaikalia2/3

19/05/1924* (code: 50869)

SERBIA, Banatsko1/2



SLOVAKIA, Dobra2/3

19/07/1969* (code: 54310)

SPAIN, Charca del Po, Seros, Leida1/2



SPAIN, Barbate, Cadiz1



SPAIN, El Puerto de Santa Maria, Cadiz1/2



TUNISIA, El Hisiane1/2/3



TUNISIA, Metbassta1/2/3



TUNISIA, Route Gafsa-Kairouan1/2/3



TUNISIA, Oum Dhouil, Cap Bon1/2/3



TUNISIA, Route Tunis2/3



TUNISIA, Raoued2



UKRAINE, Lukyanovka District, Kiev3

−/−/1913* (code: 10540)

Sample codes for Tunisian populations refer to Marrone et al. (2016). Sample codes for Apulian (Italy) sites refer to Alfonso (2017)

1 = analysed molecularly, 2 = analysed for cyst morphology, 3 = analysed for male second antenna structure; * Zoological Institute of Russian Academy of Sciences collection

Molecular analysis

Total genomic DNA was extracted from single specimens using 150–200 μl of Chelex suspension (6%, Bio-Rad Laboratories, CA, USA) with proteinase K (20 mg/ml) pre-treatment (Estoup et al., 1996). Parts of the 12S and 16S rRNA mitochondrial regions were amplified using the universal primers SR-J14197 and SR-N14745 (Simon et al., 1994) and L2510 and H3080 (Palumbi, 1996), respectively. PCR protocols were those described in Baxevanis & Abatzopoulos (2004), while sequencing protocols were adapted from Baxevanis et al. (2006). All amplifications were performed with Taq DNA polymerase (Expand High FidelityPLUS PCR System, Roche) on a Techgene (TECHNE, Cambridge, England) thermal cycler while sequencing reactions were electrophoresed on a PRISM 3730xl DNA analyzer (Applied Biosystems).

We used BioEdit (Hall, 1999) to process chromatograms and assemble sequences and Clustal X 1.8 (Thompson et al., 1997) for alignment using default parameters. BLAST searches were also conducted to confirm sequence identity. All sequences were deposited in GenBank (12S: KY385557-KY385572, 16S: KY385573-KY385624). Genetic diversity indices were calculated in MEGA version 7 (Kumar et al., 2016). For phylogenetic analysis, BEAST 1.5.3 (Drummond & Rambaut, 2007) was used on the concatenated alignment. The best-fit substitution model (TrN + G + I, the same for both 12S and 16S) was determined by jModelTest 0.1.1 (Posada, 2008) using the ΑIC (Akaike, 1974). A coalescent constant size prior was placed on the tree. Two independent Markov Chain Monte Carlo analyses were run for 10 million generations (sampling every 1000, first two million generations were discarded as burnin). Tracer v1.5.0 (Drummond & Rambaut, 2007) was used for diagnosing convergence and summarizing statistics (for each MCMC analysis separately). The adequacy of mixing was determined by checking whether the ESS (Effective Sample Size) parameter values were higher than 200. Data produced by the two independent runs were combined with LogCombiner v1.5.2, and TreeAnnotator v1.5.2 was used to find the best-supported tree.

We used the Isolation by Distance Web Service v.3.23 ( (Jensen et al., 2005) in order to test for a possible correlation between geographic and genetic distance (Kimura 2-parameter) matrices. Tests were also performed on the log-transformed values. We excluded the “S. tor” sequence by Daniels et al. (2004) (see Fig. 1) since it originates from an unknown locality.
Fig. 1

Bayesian phylogeny of 15 S. torvicornis populations based on the concatenated 12S/16S alignment. Posterior probability values >0.60 are shown. Geographical origin of sequences in each group is indicated. T. pla = outgroup sequence of Thamnocephalus platyurus Packard, 1877 (12S: AY519816, 16S: AF209057). S. tor = the only available 12S GenBank sequence (AY519814) of Streptocephalus torvicornis by Daniels et al. (2004)

Cyst morphology

An average of 20 gravid females per site were isolated individually in Falcon tubes, brought to the laboratory and kept in culture until deposition. A sample of 50 cysts per population, from randomly collected clutches of freshly deposited cysts, was examined. The cysts were rinsed clean in demineralized water and checked for quality under a stereomicroscope. They were then mounted on stubs and gold-coated for SEM morphology (see Mura, 1992; Mura & Rossetti, 2010) and photographed using an EVO LEO 040 electron microscope. All SEM observations were performed under the same light conditions to avoid undesired distortions on the images. Deformed or damaged specimens were not included in the sample.

Male second antenna structure

A total of 54 males from 15 populations were analysed for second antenna structure based on criteria used by Thiéry (1987) and Dumont et al. (1991, 1995) to distinguish S. torvicornis torvicornis and S. torvicornis bucheti. A number of 16 morphological features related to the thumb, the denticles on the thumb and the anterior peduncle (in addition to body length) were examined (see supplementary file “biometry_S. torv_males.pdf”) after tissue cleaning with hot lactic acid. The matrix with the morphological features was analysed with a cluster analysis performed with the program Primer 6 plus (Clarke & Gorley, 2006). The cluster mode was “group average” performed on a Bray–Curtis similarity matrix.


Phylogenetic analysis

The total alignment length of the concatenated 12S/16S dataset was 917 bp, with 204 and 71 variable and parsimony-informative sites, respectively. For 12S, interpopulation Kimura-2 parameter distances ranged from as low as 0.4–7.7%, with an average of 3.9%. The highest values concerned comparisons of the Iranian population (TAP) with all other populations. The same pattern was evident for 16S, with values ranging from 0.2 to 2.9% and a mean of 2.0%. The isolation-by-distance tests revealed no significant correlation (Z = 4394.04, r = 0.16, p = 0.92) between geographic and genetic distances. The phylogenetic relationships of the sampled S. torvicornis populations are shown in Fig. 1. The tree is mostly unresolved with few groups showing posterior probability values >0.60. The populations of San Donaci (DON, Apulia, Italy), Qum Tappeh (TAP, Iran) and Banatsko (BAN, Serbia) are the only ones forming coherent groupings of indigenous haplotypes. Overall, the genetic variability observed among S. torvicornis populations is geographically unpatterned.

Cyst surface pattern

Representative pictures of cyst surface ornamentation from all examined populations are shown in Figs. 2, 3, 4, and 5. A significant amount of phenotypic homogeneity is evident. For example, a “global pattern” of cysts characterized by a rather irregular spherical shape ornamented by a continuous network of ribs forming polygonal areas with raised ridges is shared by nearly all European populations (see Fig. 2; photos 1–7 in Fig. 3; photos 1–5 in Fig. 4). However, a number of notable exceptions exist. These include i) the Transbaikalia cysts (photos 8–9 in Fig. 3) with thinner ridges, ii) the very characteristic Iranian morphotype (photo 10 in Fig. 3) with a more regular spherical shape, less pronounced ridges, an absence of polygonal areas and a smooth rounded surface and iii) the Tremiti and Tunisian morphotype, quite similar to the Iranian pattern but less wrinkled and porous (photos 6–7 in Figs. 4, 5).
Fig. 2

SEM images of cysts from population Charca del Po, Spain

Fig. 3

SEM images of cysts from European and Asian S. torvicornis populations

Fig. 4

SEM images of cysts from populations of Morocco and the Mediterranean

Fig. 5

SEM images of cysts from Tunisian S. torvicornis populations

Male second antenna morphology

The analysis of 16 male second antenna structures and body length from 15 S. torvicornis populations resulted in the groupings shown in Fig. 6. Again, no clear geographic patterning can be discerned. The most divergent and coherent grouping is formed by the Slovakian population. Then, two major clusters are evident, both “paraphyletic” in terms of their composition: the first is composed of different populations from Tunisia and Apulia, while the second contains populations from Tunisia, Iran, Russia, Ukraine and Georgia. It is interesting to note that the Iranian population appears to be the strongest (or nearly so) grouping across all different markers (12S/16S, cyst morphology, male second antenna).
Fig. 6

Bray–Curtis distance of S. torvicornis populations based on the body length and 16 male second antenna characters


We have tried to investigate the phylogeography of the fairy shrimp Streptocephalus torvicornis across its circum-Mediterranean and Eurasian distribution. For that, we assembled three different datasets by sampling for genetic variation, cyst morphotypes and male second antenna structures from the species variability pool. A drawback of our study is that the three different datasets are independent and bear limited correspondence, which was due to the different fixation, composition and size of the available samples. However, they can arguably be seen from a statistical angle, taken as instances of independent samplings in order to assess the amount of existing polymorphism. In addition, the mechanisms driving the monopolization of resources in inland aquatic settings are strong, rapid and penetrative, registering sharp genetic and phenotypic discontinuities. In that sense, and despite the lack of correspondence in our datasets, we would expect to recover patterns similar to those observed in the majority of inland zooplankters. Yet, remarkably this has not been the case here. The picture we obtained for the Streptocephalus torvicornis populations is that of extensive genetic and phenotypic homogeneity, indicative of widespread connectivity and unhindered gene flow. This pattern is consistent across all three datasets.

Evidence for weak phylogeographic structure and lack of dispersal limitation has been reported previously in North American populations of Branchinecta lynchi Eng, Belk & Eriksen, 1990 (Aguilar, 2011), in Australian Limnadopsis Spencer & Hall, 1896 species (Schwentner et al., 2012) and in crustacean zooplankton communities of Ontario, Canada (Audet et al., 2013). Putting aside the geographic and ecological particularities in each case, the key feature in those studies is that effective gene flow is actually realized. In other words, successful colonization has taken place. This stands in stark contrast with the expectations of the Monopolization Hypothesis where establishment of immigrant lineages is halted soon after the first colonization of a habitat. As the massive amount of evidence points towards a regionalism biogeographical model (see Incagnone et al., 2015 and references therein) coupled with substantial population fragmentation, the presence of a few cases defying this pattern is both intriguing and enigmatic.

Based on our findings and in an effort to avoid untenable inferences, we may identify a number of factors giving rise to the observed pattern of limited population differentiation and widespread lineage occurrence in Streptocephalus torvicornis. First, Rogers (2015) has reported cases where high dispersal frequency may match or overwhelm the ability of a population to maintain resource monopolization. This may result in a constant influx of new lineages from different sources, thus delaying or even cancelling priority effects. Second, at the very early stages of colonization, secondary immigrants are offered an outbreeding vigour opportunity leading to an increase in their frequency and possible establishment (Ortells et al., 2014). However, this mechanism cannot be maintained in the long term unless stochastic extinctions or intermediate hydroperiod length periodically reset it. Third, Streptocephalus torvicornis may constitute an example of a “general-purpose genotype” able to exploit a broad ecological niche. This has been hypothesized in order to explain the wide distribution of tri- and tetraploid Artemia parthenogens (Maniatsi et al., 2011). Although Streptocephalus torvicornis has been considered as a warm stenotherm, its distribution covers quite different climatic zones (e.g. Slovakia versus Morocco in our study). Under this hypothesis, the ecological equivalence of genotypes may generate an immigration–extinction equilibrium in the long term buffering genetic diversity over spatial scales. Forth, life-history features of organisms may greatly determine rates of effective dispersal. For example, due to their mode of reproduction, parthenogenetic taxa (Maniatsi et al., 2011) are more efficient colonizers compared with gonochoristic species which typically show pronounced endemicity (e.g. Ketmaier et al., 2008; Maniatsi et al., 2009). Our results on Streptocephalus torvicornis are at odds with this pattern. However, evidence from the notostracan Triops mauritanicus (Korn et al., 2010) shows that effective colonization through migratory birds may be enhanced in open habitats as opposed to ponds surrounded by forests or shrub. Fifth, the pattern of genetic homogeneity in Streptocephalus torvicornis may reflect a shallow population history. It is very likely that European Streptocephalus populations had little time for differentiation following recent expansion from available refugia after the end of the Würm III glaciation. This scenario is in accordance with the discussion by Dumont et al. (1995) on the historical biogeography of Streptocephalus torvicornis as well as with evidence for the existence of distinct relevant refugia (i.e. Iberia, Italy, Balkans, Carpathians; see Provan & Bennett, 2008) and the extent of permafrost during that time. However, given the limitations of the markers used here, more informative DNA regions should be used to confidently address this interesting hypothesis.

Regarding the morphological partitions previously proposed by Thiéry (1987) and Dumont et al. (1991, 1995) within S. torvicornis, the distinction between the two presumed subspecies S. torvicornis torvicornis and S. torvicornis bucheti [varieties according to Alonso (1996)] appears weak and not convincing. In addition, the male second antennae features revealed to be highly variable even in the same population, and sometimes in the same specimen (right antenna was different from the left one in some specimens) and, thus, they cannot be considered a morphological feature strong enough to identify the two presumed subspecies.

Our study has admittedly some limitations. Yet, as a snapshot of the current genetic and phenotypic diversity in Streptocephalus torvicornis it reveals an unexpected pattern of homogeneity and an absence of prominent interpopulation gaps. Our findings need to be carefully tested by future work incorporating additional taxon and gene sampling complemented with abiotic and biotic metadata in a rigorous analytical framework.



This article is dedicated to the memory of Graziella Mura who initiated the Streptocephalus project, coordinated it passionately but regrettably did not manage to see it complete. She has been a real friend and a mentor for all of us and we will always remember her. We would like to thank Dani Boix (University of Girona), Massoud Seidgar (University of Teheran), Juan Garcia de Lomas (University of Cadiz), Brigita Petrov (University of Belgrade), László Demeter (Sapientia Hungarian University of Transylvania) and Stanislaw Malavin (Russian Academy of Sciences, Saint Petersburg) for kindly providing samples.

Supplementary material

10750_2017_3203_MOESM1_ESM.pdf (38 kb)
Measurements of body length and 16 morphological characters of the male second antenna (biometry_S.torv_males.pdf) (PDF 37 kb)


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Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Ilias Kappas
    • 1
  • Graziella Mura
    • 2
  • Dimitra Synefiaridou
    • 1
    • 3
  • Federico Marrone
    • 4
  • Giuseppe Alfonso
    • 5
  • Miguel Alonso
    • 6
  • Theodore J. Abatzopoulos
    • 1
  1. 1.Department of Genetics, Development & Molecular Biology, School of BiologyAristotle University of ThessalonikiThessalonikiGreece
  2. 2.Department of Animal and Human BiologyUniversity of Rome “La Sapienza”RomeItaly
  3. 3.Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, Centre for Synthetic BiologyUniversity of GroningenGroningenThe Netherlands
  4. 4.Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e FarmaceuticheUniversità di PalermoPalermoItaly
  5. 5.University of Salento – Di.S.Te.B.A.LecceItaly
  6. 6.Department of Ecology, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain

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