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Biosyst. Divers., 25(4)
Biosystems
Diversity
ISSN 2519-8513 (Print)
ISSN 2520-2529 (Online)
Biosyst. Divers., 25(4), 323–327
doi: 10.15421/011749
COXI based phylogenetic analysis of Caucasian clade
of European Troglocaris (Crustacea: Decapoda: Atyidae)
with the suggestion of a new taxonomic group structure
I. Marin
A. N. Severtzov Institute of Ecology and Evolution of RAS, Moscow, Russia
Altai State University, Barnaul, Russia
Article info
Received 19.10.2017
Received in revised form
11.11.2017
Accepted 15.11.2017
A. N. Severtzov Institute of
Ecology and Evolution of RAS,
Leninsky prospect, 33,
Moscow, 119071, Russia.
Altai State University,
Leninsky Prospect, 61,
Barnaul, 656049, Russia.
Tel.: +7-915-302-50-12
Email:
coralliodecapoda@mail.ru,
vanomarin@yahoo.com
Marin, I. (2017). COXI based phylogenetic analysis of Caucasian clade of European Troglocaris (Crustacea:
Decapoda: Atyidae) with the suggestion of a new taxonomic group structure. Biosystems Diversity, 25(4), 323–327.
doi:10.15421/011749
New genetic data on Caucasian troglobiotic shrimps collected from the territory of Russia, Abkhazia and Western
Georgia are presented. Based on new genetic data on the marker region of subunit I of cytochrome oxidase of
mitochondrial DNA (COXI mtDNA) of Caucasian species and other taxa of European cave shrimps (Troglocaris s.l.)
from GenBank (NCBI) database, a new generic structure is presented. Based on a significant genetic divergence of
COXI mtDNA subgenera of Troglocaris s.l., namely Troglocaris s.s., Xiphocaridinella and Spelaeocaris, should be
considered as separate genera while Troglocaris (Troglocaridella) hercegovinensis (Babić, 1922) is suggested to be
transferred within Dinaric genus Spelaeocaris as Spealeocaris hercegovinensis (Babić, 1922) comb. nov. Besides,
Troglocaris bosnica shows a significant a genetic difference (at the level of the separate genus) from the remaining
representatives of the genus Troglocaris s.s. Moreover, p-distances (COXI) of about 17% are supposed for generic
separation within European Troglocaris-related atyid shrimps and 5% for separation of cryptic species within Caucasian
Xiphocaridinella. A list of all known taxa of Troglocaris-related atyid shrimps of the European part and a discussion of
the general distribution of troglocaridid atyid shrimps in the Balkans and the Caucasus are presented. A new version of
divergence events between Dinaric–Caucasian Troglocaris lineages (genera) based on new genetic data is suggested.
Keywords: phylogeny; COXI mtDNA; Xiphocaridinella; stygobiotic; stygobionts; shrimps; Caucasus
Introduction
Karst biocenoses due to their isolated location are especially
rich in endemic species. It is very likely that each karst system has
its own unique set of inhabiting species. One of the richest troglo-
biotic faunas in the world exists on the territory of the Southern
Caucasus, followed by the cave and underground water fauna of the
Balkan Peninsula. At the same time, the degree of study of the
European hypogean communities obviously considerably exceeds
that of the Caucasian ones. Troglobiotic higher crustaceans (Deca-
poda, Isopoda and Amphipoda) are the most important component
of the hypogean cave ecosystems, sometimes forming them entire-
ly. As a rule, in cave associations, crustaceans lead in number and
diversity, forming the basis of the food pyramid of these commu-
nities. The relatively sparse data from the karst regions of the Cau-
casus indicate the extreme richness of the fauna of 37 troglobiotic
crustaceans (about 50 endemic species in the Caucasus are known)
(see review in Turbanov and Marin, 2015; Turbanov et al., 2016).
At the moment, both the habitation of a larger number of species,
and the wider distribution of this group in the Caucasus are assu-
med (e.g. Sadowsky, 1930; Birštein, 1939, 1948; Juzbaš’jan, 1940;
Sendra and Reboleira, 2012; Marin and Sokolova, 2014; Marin,
2017; Turbanov et al., 2016). At the same time, subterranean fauna
is characterized by a large number of endemics (local endemism),
due to special ecological conditions and isolated location and low
potential for dispersal (see Sket and Zakšek, 2009).
The European stygobiotic atyid shrimp genus Troglocaris Dor-
mitzer, 1853 (Crustacea: Decapoda: Atyidae) is currently divided
into 4 subgenera: Spelaeocaris Matjašič, 1956 (4 species), Troglo-
caridella Babić, 1922 (1 species), Xiphocaridinella Sadowsky, 1930
(6 species) and Troglocaris s. str. (4 valid species and 6 subspecies)
(Zakšek et al., 2006, 2009; Sket and Zakšek, 2009; Marin and So-
kolova, 2014; Marin and Turbanov, 2015; Marin 2017; Marin and
Sinelnikov, 2017). The main morphological peculiarity which dis-
tinguishes Troglocaris from other European atyid shrimps, such as
Atyaephyra de Brito Capello, 1867, Dugastella Bouvier, 1912,
Gallocaris Sket et Zakšek, 2009 and Typhlatya Creaser, 1936 (Sket
and Zakšek, 2009) is the length of the subapical and apical spines
on the appendix masculina in males, which are significantly smaller
than the diameter of the appendix masculina in all representatives of
the genus Troglocaris (see key in Sket and Zakšek, 2009). At pre-
sent, the division into subgenera does not satisfy modern morpholo-
gical requirements, since most of the considered morphological fea-
tures vary greatly even within the species of the same subgenus
(see, for example, the length of the rostrum within the subgenus of
Xiphocaridinella (see Marin, 2017)) and such division is mainly
supported by geographical distribution.
Order Decapoda Latreille, 1802
Family Atyidae De Haan, 1849
Subfamily Typhlatyinae Holthuis, 1986
Genus Troglocaris Dormitzer, 1853
Subgenus Troglocaris Dormitzer, 1853 – distributed exclusively in the Balkans
Troglocaris (Troglocaris) anophthalmus (Kollar, 1848)
Troglocaris (Troglocaris) anophthalmus anophthalmus (Kollar, 1848)
Troglocaris (Troglocaris) anophthalmus intermedia Babić, 1922
Troglocaris (Troglocaris) anophthalmus legovici Jugovic, Jalžić, Prevor-
čnik and Sket, 2012
Troglocaris (Troglocaris) anophthalmus ocellata Jugovic, Jalžić, Prevor-
čnik and Sket, 2012
323
Biosyst. Divers., 25(4)
Troglocaris (Troglocaris) anophthalmus periadriatica Jugovic, Jalžić,
Prevorčnik and Sket, 2012
Troglocaris (Troglocaris) anophthalmus sontica Jugovic, Jalžić, Prevor-
čnik and Sket, 2012
Troglocaris (Troglocaris) bosnica Sket et Zakšek, 2009
Troglocaris (Troglocaris) planinensis Birstein, 1948
Troglocaris (Troglocaris) schmidti Dormitzer, 1853
Subgenus Spelaeocaris Matjašič, 1956 – distributed exclusively in the Balkans
Troglocaris (Spelaeocaris) kapelana Sket et Zakšek, 2009
Troglocaris (Spelaeocaris) neglecta Sket et Zakšek, 2009
Troglocaris (Spelaeocaris) prasence Sket et Zakšek, 2009
Troglocaris (Spelaeocaris) pretneri (Matjašič, 1956)
Subgenus Troglocaridella Babić, 1922 – distributed exclusively in the Balkans
Troglocaris (Troglocaridella) hercegovinensis (Babić, 1922)
Subgenus Xiphocaridinella Sadowsky, 1930 – exclusively Caucasian group
Troglocaris (Xiphocaridinella) ablaskiri Birstein, 1939
Troglocaris (Xiphocaridinella) fagei Birstein, 1939
Troglocaris (Xiphocaridinella) jusbaschjani Birstein, 1948
Troglocaris (Xiphocaridinella) kutaissiana (Sadowsky, 1930)
Troglocaris (Xiphocaridinella) osterloffi Juzbaš’jan, 1940
Troglocaris (Xiphocaridinella) kumistavi Marin, 2017
The active study of cave shrimps in the Caucasus began in the
1930s–1950s. At the moment, 6 species of the genus Troglocaris
(subgenus Xiphocaridinella) are described from the caves from the
territory of the southwestern part of Russia, Abkhazia and Western
Georgia, which are relicts of the freshwater fauna of the Sarmatian
or Pontine seas (basins) (Sadowsky, 1930; Birštein, 1939, 1948;
Juzbaš’jan, 1940; Sendra and Reboleira, 2012; Marin and Sokolo-
va, 2014; Marin, 2017). This group is assumed to be much more
diverse in the Caucasus than is presently known and many species
will be discovered in the nearest future. Shrimps of the genus Trog-
locaris have been recorded at a depth of more than 2,000 meters in
the lower siphon of Krubera Cave in Abkhazia, which at the mo-
ment is considered the deepest in the world (Sendra and Reboleira,
2012). To mark species within crustacean genera, including the
Troglocaris (Xiphocaridinella) species complex, it is useful to use
the mitochondrial cytochrome c oxidase subunit I gene marker
(COI), as one of the most informative markers for population and
species-level genetic studies (Avise, 1993). At the same time, data
on the Caucasian clade are not numerous and special criteria are
needed for recognition of species and genera within this group of
atyid cave shrimps.
Material and methods
This paper presents an attempt to evaluate the genetic diversity
on the marker region of subunit I of cytochrome oxidase of
mitochondrial DNA (COXI mtDNA) of troglobiotic shrimps of the
genus Troglocaris and representatives of the genus from the Cauca-
sus based on available collections and new collected material. For
the Caucasian clade freshly collected topotypic material was used,
which allowed us to obtain genetic data that had not previously
been reported for this genus – Troglocaris (Xiphocaridinella) kuta-
issiana Sadowsky, 1930 (Tskaltsitela Cave, Western Georgia),
Troglocaris (Xiphocaridinella) fagei Birštein, 1939 (New Athon
Cave, Abkhazia), Troglocaris (Xiphocaridinella) jusbaschjani Bir-
štein, 1948 (Agura River, Sochi, Russia), Troglocaris (Xiphocari-
dinella) ablaskiri Birštein, 1939 (Abrskila Cave, Abkhazia) and
Troglocaris (Xiphocaridinella) osterloffi Juzbaš'jan, 1940 (the Lower
Shakuran Cave, Abkhazia) and Troglocaris (Xiphocaridinella) ku-
mistavi Marin, 2017 (Prometheus (Kumistavi) Cave, Western Geor-
gia). The name "Troglocaris birsteini Muge, Zueva et Ershov, 2001",
proposed for the species reported from Otapa Cave, should be con-
sidered as nomen nudum (Franjevic et al., 2010). All collected ma-
terial is deposited in the collection of the Laboratory of Ecology and
Morphology of Marine Invertebrates of the Institute of Ecology and
Evolution. A. N. Severtsov RAS (Moscow). Species names and a
modern taxonomic position are given according to the international
database of the World Register of Marine Species (WoRMS) and
the Marine Species Identification Portal.
To resolve the taxonomy of cryptic diversity of species comp-
lex fragments of the mitochondrial gene coding for cytochrome
oxidase c subunit I (COI) as one of the most popular markers for
population genetic studies (Avise, 1994, 2000) were amplified and
compared. Total genomic DNA was extracted from pleopods or
abdominal muscle tissue using the innuPREP DNA Micro Kit
(AnalitikJena, Germany) following the manufacturer’s protocol. The
mitochondrial marker COI was amplified with the help of «PCR
Core» (Isogene Lab., Moscow) using the universal primers LCO1490
(5'-ggtcaacaaatcataaagatattgg-3') and HC02198 (5'-taaacttcagggtga-
ccaaaaaatca-3') (Folmer et al., 1994). PCR products were performed
on amplificator «Tercik DNA Technology» under the following
conditions: initial denaturation at 94 °C for 2 min followed by 40
cycles of 95 °C for 2 min, 59°C for 45 s, and 72 °C for 1.5 min,
followed by chain extension at 72 °C for 7 min. The volume of 20 uL
of reaction mixture contained 5 uL of total DNA, 10 uL of PCR
Diluent and 2.5 uL of each primer. Synthesis of the full-length
fragment was performed at an annealing primer temperature 59 °C
during 45 seconds. The amplification products were separated by
using gel electrophoresis of nucleic acids on a 2% agarose gel in
1xTBE, and then stained and visualized with 0.003% EtBr using
imaging UV software. The resulting PCR products were sequenced
in both forward and reverse direction on the basis of "EuroGen"
(Moscow, Russia). Uniformity of sequences obtained was perfor-
med using the program BioEdit v. 5.0.9. The resulting markers of
COXI gene of mtDNA with 598 bp long section were used for
further phylogenetic analysis. The received nucleotide alignments
of COI gene were used to construct the phylogenetic relations (tree)
in MEGA 7.0 using k-nearest neighbor’s algorithm (k-NN, Neigh-
bor-Joining method) and Maximum-likelihood algorithm. Uncor-
rected pairwise genetic distances (p-distance) were calculated based
on COI sequences using MEGA 7.0. Data on “molecular clocks”
are used according to Zakšek et al. (2006) calculated for Troglocaris
s.s. as well as Knowlton et al. (1993) and Knowlton & Weigt (1998)
suggested for shrimps of the genus Alpheus (Crustacea: Decapoda:
Alpheidae) as sequence divergence rate of about 1.4–2.4% per
MYA for COXI gene marker.
Results
All known Caucasian Xiphocaridinella species are strictly
restricted to certain karst cave ecosystems showing significant genetic
divergence between known species (Table 1), which is usually not
less than 5%. At the same time, the interspecies genetic variability
within populations is very low (Table 2). Relatively high variability
within Troglocaris (Xiphocaridinella) fagei is explained by mixture
of three separate populations from the closely spaced New Athon,
Habu and Mchishta сaves, while variability within population from
each of caves is similar to other species, being about 0.003
substitutions per 100 nucleotides.
Table 1
Uncorrected pairwise genetic (COXI) distances between known Caucasian species of subgenus Xiphocaridinella
(asterisk indicates minimum values of p-distances)
Species X. kutaissana X. kumistavi X. ablaskiri X. osterloffi X. fagei
X. kumistavi 0,058 ± 0,010* – – – –
X. ablaskiri 0,112 ± 0,014 0,099 ± 0,013 – – –
X. osterloffi 0,120 ± 0,014 0,108 ± 0,013 0,103 ± 0,014 – –
X. fagei 0,120 ± 0,014 0,107 ± 0,014 0,106 ± 0,014 0,100 ± 0,013 –
X. jusbachiani 0,109 ± 0,014 0,104 ± 0,015 0,104 ± 0,015 0,108 ± 0,014 0,064 ± 0,010*
324
Biosyst. Divers., 25(4)
Table 2
Uncorrected pairwise genetic (COXI) distances within studied
populations of known Caucasian species of subgenus Xipho-
caridinella (asterisk indicates minimum values of p-distances)
Species Uncorrected pairwise genetic
Xiphocaridinella fagei 0,014 ± 0,003*
X. kutaissana 0,0006 ± 0,0006*
X. ablaskiri 0,003 ± 0,001
X. jusbachiani 0,002 ± 0,001
X. osterloffi 0,003 ± 0,0015
X. kumistavi 0,0009 ± 0,0008*
Uncorrected pairwise genetic (COXI) distances (p-distances)
between subgenera of Troglocaris s.l. (Table 3; Fig. 1) show well
supported divergences with p-distances not less than 17–20%. The
division of the subgenus Spelaeocaris and Troglocaridella for the
Dinaric group is not justified on the basis of available molecular
data. The genetic subdivision between subgenera of Troglocaris s.l
is similar to generic level divergence between Galocaris and Trog-
locaris s.s. (Table 3). The data obtained clearly support the mono-
phylety of Xiphocaridinella and Troglocaris s.s. while Spelaeocaris
represents a paraphyletic taxon (Fig. 1).
Discussion
The genetic subdivision between subgenera of Troglocaris s.l is
similar to generic level divergence between Galocaris and Troglo-
caris s.s (Table 3). Such phylogenetic relations within Troglocaris
are also supported by Sket and Zakšek (2009) based on sequences
of cytochrome oxidase subunit I (COI) + 16S rDNA. Thus, subge-
nera of the genus Troglocaris s.l. should be considered as separate
genera. It is possible to use p-distances calculated for COXI gene
marker larger than 17% for generic separation within European
Troglocaris-related atyid shrimps and 5% for separation of cryptic
species within Caucasian Xiphocaridinella, which is rather similar
to criteria suggested in other groups of decapod crustaceans and
invertebrates (see Knowlton et al., 1993; Knowlton and Weigt, 1998;
Hebert et al. 2003; Sites and Marshall 2004; Zakšek et al., 2006,
2009; Lefébure et al. 2006; Lushai et al., 2003). Besides, Trogloca-
ris bosnica shows a significant genetic difference (at the level of the
separate genus) from the remaining representatives of the genus
Troglocaris s.s. (Table 3).
At the same time, the monotypic genus Troglocaridella is sepa-
rated from the representatives of the genus Spelaeocaris mostly
based on the presence of supraorbital spines on the carapace in
T. hercegovinensis vs. their absence in Spelaeocaris (after Sket and
Zakšek, 2009). Such morphological features are variable within
genera (Sket and Zakšek, 2009; Marin and Sokolova, 2014) while
generic data (Fig. 1; Table 3) do not allow clear separation of
T. hercegovinensis from other representatives of the genus Spe-
laeocaris and it is presently suggested to synonymize genera
Spealeocaris and Troglocaridella of the Dinaric group and further
consider the species as Spealeocaris hercegovinensis (Babić, 1922)
comb. nov.
Table 3
Uncorrected pairwise genetic (COXI) distances between subgenera of Troglocaris s.l. and outgroup atyid shrimp genera
(asterisk indicates minimum values of p-distances)
Species Troglocaris Troglocaris
bosnica Spealeocaris Troglocaridella Xiphocaridella Atyaephyra Dugatella Galocaris
Troglocaris bosnica 0,153 ± 0,024* – – – – – – –
Spealeocaris 0,217 ± 0,024 0,222 ± 0,024 – – – – – –
Troglocaridella 0,243 ± 0,024 0,241 ± 0,025 0,169 ± 0,024* – – – – –
Xiphocaridella 0,214 ± 0,024 0,225 ± 0,024 0,189 ± 0,025* 0,207 ± 0,024 – – – –
Atyaephyra 0,265 ± 0,027 0,261 ± 0,029 0,295 ± 0,027 0,322 ± 0,031 0,275 ± 0,020 – – –
Dugatella 0,264 ± 0,022 0,279 ± 0,026 0,287 ± 0,024 0,308 ± 0,026 0,296 ± 0,017 0,275 ± 0,018 – –
Galocaris 0,200 ± 0,025* 0,213 ± 0,023 0,276 ± 0,025 0,295 ± 0,026 0,255 ± 0,020 0,257 ± 0,025 0,260 ± 0,021 –
Typhlatya 0,275 ± 0,023 0,264 ± 0,020 0,260 ± 0,023 0,290 ± 0,023 0,289 ± 0,018 0,255 ± 0,023 0,288 ± 0,019 0,235 ± 0,016
Fig. 1. The evolutionary tree of Troglocaris s. l. based on COXI gene marker obtained
using the Maximum–Likelihood method based on the Kimura 2–parameter model
325
Biosyst. Divers., 25(4)
Similar morphological variability in the armature of the rostrum
in the carapace is known from the Caucasian Xiphocaridinella cur-
rently including 6 valid species known from the Russian part of the
Caucasus (Krasnodar Territory), Abkhazia and Western Georgia.
Xiphocaridinella jusbaschjani known exclusively known from the
Agura River (Sochi, Russia) shows an extremely short (reduced)
unarmed rostrum and the absence of supraorbital or suborbital teeth
on the carapace. This has even led to the transfer of the species to the
genus Typhlatya (D'UdekemD'Acoz, 1999). Five remaing species
of Xiphocaridinella show a varying pattern of armature of the
rostrum from unarmed in X. fagei (Marin and Sokolova, 2015) to
strongly armed dorsally and ventrally in X. kumistavi (Marin, 2017).
Anyway, X. jusbaschjani strictly belongs to the genus Xiphocaridi-
nella by other morphological features and present genetic data
(Table 1; Fig. 1). Thus, the armature of the rostrum and the presen-
ce of supraorbital or suborbital teeth on the carapace could not be
considered as morphological features of the generic level. More-
over, extreme variations of the length of the rostrum and supraorbi-
tal teeth within the genera Troglocaris and Xiphocaridinella and
even populations of Troglocaris-related shrimps has been shown
(Zakšek et al., 2007; Jugovic et al., 2010, 2011, 2012; Marin, 2017),
even suggesting the theory of the influence of predators such as
cave salamander Proteus anguinus Laurenti, 1768 (Amphibia: Cau-
data: Proteidae) (Jugovic et al., 2011). The obtained genetic data
clearly support the monophylety of Xiphocaridinella and Trogloca-
ris while Spelaeocaris represent a paraphyletic taxon (Fig. 1).
It is obvious that representatives of modern genera Troglocaris,
Spelaeocaris and Xiphocaridinella were descended from a common
ancestor which lived in the ancient Sea of Paratethis. The hypothe-
sis of the recent split (about 6–11 million years ago) between the
Caucasian and Dinar cave shrimps of the Paratethis relict (Zakšek
et al., 2006) supports the idea of a closer relationship between the
subgenus Spelaeocaris and Xiphocaridinella than with the Dinaric
group, which we also believe is correct on the basis of our research.
Besides, it is possible to suggest two separate divergence events
between within Dinaric–Caucasian Troglocaris lineages (genera) ,
which occurred about 9–15MYA (ancestors of Troglocaris separa-
ted from Spelaeocaris–Xiphocaridinella) and about 8–13MYA when
ancestors of Spelaeocaris separated from Troglocaris vs single split
about 6–11MYA suggested by Zakšek et al. (2006).
Author is very thankful to Dr. Roman S. Dbar (Institute of Ecology of Aca-
demy of Science of Abkhazia) for help during sampling in Abkhazia, to
Dr. Pavel Sorokin (A. N. Severtzov Institute of Ecology and Evolution of
RAS, Moscow) for help with sequencing and Ilya Turbanov (I. D. Papanin
Institute for Biology of Inland Waters of Russian Academy of Sciences, Bo-
rok, Russia) for help during sampling in Otap and Abrskil caves and collec-
ting the specimens in Samschitovaya Cave.
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