Possible species-flock scenario for the evolution of the cyprinid genus Capoeta (Cypriniformes: Cyprinidae) within late Neogene lake systems of the Armenian Highland
Possible species-flock scenario for the evolution of the cyprinid genus Capoeta (Cypriniformes: Cyprinidae) within late Neogene lake systems of the Armenian Highland
Anna AyvazyanID 0 1
Davit VasilyanID 1
Madelaine B o?hme 0 1
0 Department of Geosciences, Eberhard-Karls-University T u ?bingen , T u ?bingen, Germany, 2 Senckenberg Center for Human Evolution and Palaeoenvironment (HEP), T u ?bingen, Germany, 3 JURASSICA Museum, Porrentruy , Switzerland , 4 Department of Geosciences, University of Fribourg , Fribourg , Switzerland
1 Editor: Ju ?rgen Kriwet, University of Vienna , AUSTRIA
We studied 4 Ma old isolated pharyngeal teeth from lake sediments of C?evirme (Tekman Palaeolake, Erzurum Province). Based on shape characters defined for 3D models of modern species, we found that the Pliocene lake constitutes sympatric occurrence of four Capoeta species (C. cf. umbla, C. cf. baliki, C. cf. sieboldi and C. sp. sevangi/capoeta), whose modern relatives belong to a monophyletic clade inhabiting today three different drainage systems of this region (Euphrates River, Kura River and Black Sea). We interpreted this high local diversity of closely related species in terms of the species-flock model. The Tekman palaeolake was a part of an unrecognized extended late Miocene to Pliocene palaeolake system in the present-day Armenian Highland, which has been disrupted by Pliocene tectonic activities. Surface uplift of the Armenian Highland contributed to the very characteristic biogeographic distribution and endemism of Capoeta in West Asian drainage systems. Thus, we proposed a species-flock scenario for the evolution and dispersal of the cyprinid genus Capoeta in a huge unrecognized palaeolake system in the present-day Armenian Highland.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: This study was funded in part by the
German Academic Exchange Service (DAAD), ID:
57076385. This scholarship (Research fellowships
for doctoral candidates and young scientists) was
awarded to AA. The funder had no role in study
design, data collection and analyses, decision to
publish, or preparation of manuscript. No
Tigris and Euphrates are the largest rivers in Western Asia, both have a rich and diverse
aquatic fauna which includes seven endemic fish genera (two of the Cobitidae family and five
of the Cyprinidae family) [
]. In southern Caucasus, the Kura-Araxes River Basin is the major
river system with many tributaries [
]. It is also characterized by several endemic fish species
]. Among them, the cyprinid genus Capoeta shows phylobiogeographical pattern and it is
widely distributed in Western Asia and the Ponto-Caspian region (Euphrates, Tigris, Araxes,
Kura and Orontes) with 30 valid species [
]. The distribution of the Capoeta species within
additional external funding was received for this
study. German Academic Exchange Service
(DAAD) website: https://www.daad.de/de/.
Western Asian and Ponto-Caspian water basins provides an excellent basis for the analyses
biogeographical evolution of the main drainage systems of this region.
Western Asia situated on the border of three continents (Europe, Asia, Africa), plays an
important role in the dispersal of different groups of organisms. The area, having complex
topography, provides various habitats and creates unique ecosystems. The territory is formed
during a long and complex geological history, driven by the tectonic convergence of the
AfroArabian and Eurasian plates [
]. Despite its biogeographic bridging position between the
Palearctic, Afrotropic and Indomalaya realms, its deep-time biodiversity has not been studied,
hampering comprehensive interpretation of the present diversity and its potential role in
evolutionary processes. Western Asian and Ponto-Caspian drainage system include rather short
and small but numerous drainage systems of the Mediterranean Sea Basin (this territory
includes southern Anatolia, Syria, Lebanon, Israel, the Arabian Peninsula), Black Sea Basin
(northern Anatolia and Western Georgia), the Tigris-Euphrates (Persian Sea Basin) and
KuraAraxes basins, most of Iranian territory (Caspian Sea Basin) [
The four main rivers of Western Asia and the Ponto-Caspian region (Euphrates, Tigris,
Kura and Araxes) all originate in the Armenian Highland (Fig 1A). The history and formation
of these water basins remain largely unknown. To track the evolution of drainage basins, fossil
records of aquatic faunas can be used. Recently, Vasilyan & Carnevale (2013) shown, using the
fossil record of the genus Garra from Armenia, that area including the upper reaches of the
present-day Araxes River drainage system belonged to the Protoeuphrates-Tigris drainage
system in the latest Miocene [
] [earlier  the age of the locality has been dated to Pliocene,
the new results [
] suggest slightly older age latest Miocene].
In the present study, we trace back the fossil record of the genus Capoeta to 4 Ma, using
fossil material found at the Pliocene age locality C? evirme (Erzurum Province, Tekman district) in
Eastern Turkey (Fig 1A and 1B). The study sets the following goals: (1) to apply the established
] for species-level identification of isolated pharyngeal teeth of Capoeta; (2) to
determine species composition within the fossil sample; (3) to evaluate the history and
coverage of lacustrine sediments in Western Asia and the Ponto-Caspian region; and (4) to discuss
evolutionary models for the genus Capoeta with respect to its biogeography.
Species flock concept in ichthyology
A species flock is a monophyletic group of closely related sympatric species inhabiting the
same area or geographically restricted area. The species flock is common for both vertebrate
and invertebrate animals, which show rapid adaptive radiation, morphological divergence and
]. The examples of species flock are recorded in different groups of animals:
insects, fishes, lizards and birds, [
]. Especially monophyletic groups of fishes represent a
particular interest, as one of the criteria of the species to be considered as a species flock is the
monophyly of the described groups/species [
Two main well-known species flocks of cyprinids fishes are found in the Philippine Lake
Lanao and the Ethiopian Lake Tana [
]. Besides the extant species flocks, some
potential fossil species flocks are also reported, e.g., from the Eocene site in Tanzania, the upper
Miocene Lukeino Formation in the Tugen Hills of the Central Rift Valley of Kenya .
Cyprinid pharyngeal dentition
The oral jaws (e.g. dentary, maxilla, premaxilla) of cyprinids are toothless. Instead they have
pharyngeal teeth located on the pharyngeal bones [
]. Both left and right fifth
ceratobranchials are modified into pharyngeal jaws, which have the function of food processing [
The pharyngeal bones and teeth provide important taxonomic characters for systematics of
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Fig 1. The Armenian Highland. (a), Fossil locality marked by red contoured circle in a relation to the Euphrates-Tigris and Araxes-Kura water basins. (b), map showing
the fossil locality marked by red contoured circle. Map data: Fig 1A and 1B is redrawn and modified from U. S. Geological Survey, CC BY 4.0.
the cyprinid fishes. The number and arrangement of the pharyngeal teeth in tooth rows are
recognized and widely used diagnostic characters for cyprinid classification [
The fossil remains of cyprinids are mainly represented by isolated pharyngeal teeth [
and it is hard to identify specimens based on sole isolated teeth. Therefore, the fossil record of
many cyprinids, included the genus Capoeta, is still largely unknown.
The fossil record of the genus Capoeta
According to the molecular data, the genus Capoeta originates around the
Langhian?Serravallian boundary (13.9 Ma) and diversification within the genus occurs along the Middle
Miocene?Late Pliocene period [
The scarce fossil record of Capoeta comes from four localities, two from the late Miocene
and two from the Pleistocene. Miocene Capoeta fossils are known from Armenia and Georgia,
both in the present-day Kura-Araxes drainage basin (Fig 2). The first fossil remains of Capoeta
nuntius are described by Bogachev (1927) at the late Miocene locality in the Kisatibi,
Samtskhe-Javakheti region, Georgia [
]. The material is represented by three more or less
complete and a few strongly damaged skeletons as well as more than 70 isolated bone
fragments. Vasilyan & Carnevale (2013) describe skeletons of Capoeta sp. from the Jradzor locality
(latest Miocene) in Armenia . The record of Capoeta from late Pliocene sediments at
Ericek (Cameli Basin, SW Anatolia) is doubtful [
], since the tooth morphologies (Fig 4A?4D in
]) are not found within pharyngeal teeth of the Capoeta species. Instead of this, they
resemble the morphology of the genus Luciobarbus; as the reported cobitid and gobiid remains are
snake jawbones. Vasilyan et al. (2014) describe two isolated pharyngeal teeth and two
fragments of serrated dorsal fin rays referred to Capoeta sp. from the early Pleistocene locality
Pasinler (Erzurum Province, north-eastern Turkey). Fossil remains of Capoeta damascina
Valenciennes, 1842 are also recorded from the Hula Palaeolake [
]. The site is situated in the
northern part of the Dead Sea Rift, Israel and dated to the Middle Pleistocene (0.78 Ma).
Biogeographical distribution of extant Capoeta species
According to the molecular data, the monophyletic genus Capoeta is represented by three
main clades: Mesopotamian, Anatolian-Iranian and Aralo-Caspian clades and nested within
the genus Luciobarbus as a sister group of the species Luciobarbus subquincunciatus [
] (Fig 3A and 3B). The Mesopotamian group contains species distributed in the
TigrisEuphrates drainage system and adjacent water basins: Capoeta trutta (Heckel, 1843), Capoeta
turani O?zulu & Freyhof, 2008 and Capoeta barroisi Lortet, 1894. The Anatolian-Iranian group
includes species inhabiting the Black Sea Basin: Capoeta sieboldi Steindachner, 1864, Capoeta
baliki Turan, Kottelat, Ekmekc?i & Imamoglu, 2006, Capoeta banarescui Turan, Kottelat,
Ekmekc?i & Imamoglu, 2006. The Mediterranean drainage basins (Anatolian-Iranian clade) of
southeastern Turkey, the Tigris?Euphrates river system, and small rivers, which drain into the
gulfs of Persia and Oman, as well as inland water bodies in Iran contain the following species:
Capoeta buhsei Kessler, 1877, Capoeta saadii (Heckel, 1847), Capoeta caelestis Scho?ter, O?zulu
& Freyhof, 2009, Capoeta damascina, Capoeta angorae (Hank?, 1925) and Capoeta kosswigi
Karaman, 1969. Finally, the Aralo-Caspian group includes the species distributed in the Kura
and Araxes rivers, as well as Aral and Caspian Sea drainages: Capoeta capoeta Gu?ldensta?dt,
1773, Capoeta sevangi De Filippi, 1865, Capoeta aculeata (Valenciennes, 1844) (S1 Table) [
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Fig 2. Geographical overview of the drainage systems of Western Asia and the Ponto-Caspian regions (Euphrates-Tigris, Araxes-Kura). Red star (1) indicates the
position of the C?ev?rme locality. The red circle shows the possible extension of palaeolake system of the Armenian Highland. The arrows show the late distribution of the
recorded fossil Capoeta species into the different water basins due to the tectonic disruption of the Lake system during the Pliocene uplift period. The two already known
late Miocene fossil sites Kisatibi (red star 2) and Jradzor (red star 3) are included as well. Map data: Fig 2 is redrawn and modified from U. S. Geological Survey CC BY 4.0.
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Fig 3. Phylogeny of the genus Capoeta. (a), distinguished clades within the genus Capoeta (Luciobarbus suquincunciatus is the sister clade) (Levin et al., 2012). The
clade diagnostic shape classes of recorded clades within the fossil material (see, Ayvazyan et al. 2018; Fig 7) are given in capital letters included 3D images of teeth of
Capoeta as well as the a2 tooth of L. subquincunciatus. The monophyletic Anatolia-Iranian/Aralo-Caspian/sieboldi clade, for which we propose a species flock model of
evolution, is marked by red colour. (b), the location of Capoeta clade within phylogenetic tree based on the molecular genetic analysis (Levin et al., 2012).
A recent phylogenetic analysis [
], using the morphologies of pharyngeal teeth of ten
Capoeta species, groups them in four main clades. Three of these clades show the same tree
topography that the molecular data provides, the remaining clade groups differently [
Late Neogene lacustrine sedimentation in the Armenian Highland
Present-day Armenian Highland (Eastern Anatolia, Armenia, Iranian Azerbaijan,
SamtskheJavakheti region of Georgia) is composed of the high mountainous landscapes of the Eastern
Taurides with elevations between 1.700 to over 5.000 meters above sea level. Because of the
dominant arid climate during the late Holocene, lakes are rare in this region. Two endorheic
saline lakes, Lake Van and Lake Urmia, as well as the freshwater Lake Sevan are notable
exceptions (Figs 1A and 2). However, geologic mapping revealed, that during the pre-Quaternary
lacustrine, sedimentation was widespread and long lasting in this region. According to Alt?nl?
(1966) during the Late Miocene and Pliocene (11.6?2.6 Ma) lacustrine sedimentation
dominated Eastern Anatolia with regional thicknesses of deposits over 1.000 m. These sediments
contain a rich freshwater fauna (e.g. diatoms, gastropods, bivalvs, ostracods, fishes); [
and have been variously attributed to the Horasan Formation, Gelinkaya Formation, I??klar
Formation (all in the Erzurum Province), Z?rnak Formation (Bitlis Province), C? ayba?i
Formation (Elaz?? Province), or to the Parc?ikan Formation (Malatya Province). Despite extensive
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syn-sedimentary volcanism, none of these formations are radiometrically dated, but available
K-Ar data  and rare rodent fossils [
] suggest that the main lacustrine phase in Eastern
Anatolia centred between 6 and 3 Ma, probably coeval with the supposed uplift of this region
An older lacustrine period is documented in Iranian Azerbaijan, where fish bearing
(Atherinidae, Cyprinodontidae, Leuciscinae, but no Barbinae) lake sediments from the Tabriz Basin
(?lignite beds?, ?fish beds?) have been dated to between 12 and 7.5 Ma [
These late Neogene lacustrine sediments have tectonically fragmented exposure over a huge
area in the Eastern Taurides stretching several hundreds of kilometres, notably including the
upper reaches of present-day Euphrates, Tigris, Kura and Araxes rivers (Fig 2).
Fossil locality C? ev?rme
The fossil site C? ev?rme (Erzurum Province, Tekman district) is located 12 km west of the
Hacio?mer village on the road from Hacio?mer to Tekman, 500 m after the bridge over the
Araxes River (coordinates: N 39? 37? 37??; E 41? 38?; Figs 1A, 1B and 2). The locality belongs
to the Tekman Basin (East-Anatolian Taurides), approximately 40 km south from the Pasinler
Basin and 120 km north-northwest of Lake Van. Late Neogene sediments in the Tekman Basin
laying discordant over early Miocene marine limestones [
]. The sedimentary facies of the
basin infill change from fluvial-alluvial to lacustrine. The late Miocene sedimentary formation
(Hac?o?mer Formation) is composed of an approximately 300 m thick reddish-brown sequence
of conglomerates, sandstone and silts with minor intercalation of marls. In the south of the
basin, the alteration with vulcanites appear. These terrestrial-fluvial fossil free layers intercalate
in their upper parts with nearly 200 m thick lacustrine sediments of the I??klar Formation,
which mainly consist of light grey, as well as slightly reddish freshwater carbonates (Fig 1B).
Layers of marl, organic rich clay and tufa are also present. The section is covered by Pleistocene
basalts from the Bingo?l Dag area [
The fossil site C? ev?rme, discovered and first described by Sickenberg (1975), belongs to the
lacustrine upper part of the I??klar Formation. The 65 m thick stratigraphic section is
subdivided based on lithological and sedimentological characters. The fossil remains of fishes,
molluscs and mammals are found at 18 m depth of the section (Fig 4). Earlier palynological studies
at C? ev?rme section indicate an early Pliocene pollen spectrum, which is in accordance to the
small mammal fauna [
]. A recent preliminary taxonomic update of the rodent
association reveals, among others, the genera Mimomys and Occitanomys and a MN15a
biostratigraphic position, roughly of about 4 Ma in the middle part of the Pliocene .
Material and methods
The studied fossil fish material is collected from 1965?1969 during the prospection of Neogene
lignite deposits of Turkey [
]. The material contains 247 isolated pharyngeal teeth (Table 1,
Fig 5A?5U) collected from the early Pliocene locality C? ev?rme in Eastern Anatolia, Turkey.
From the same horizon, 41 isolated pharyngeal teeth of Leuciscinae (Leuciscus sp.) and some
amphibian and reptile bones are also founded [
]. The studied fossil material already housed
in the Bundesanstalt fu?r Geowissenschaften und Rohstoffe, Hannover (BGR collection
numbers) and no additional excavation of fossils was undertaken. The studied isolated fossil
pharyngeal teeth are photographed under the Leica DVM5000 digital microscope, Leica M50
stereomicroscope and LEO Model 1450 VP scanning electron microscope (SEM). Recent
comparative material (pharyngeal bones) is represented by adult individuals and comes from
following collections: Bavarian State Collection for Anthropology and Palaeoanatomy Munich
(SNSB), Palaeontological Collection of Tu?bingen University (GPIT), Senckenberg
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Fig 4. Sedimentary succession of the I??klar Formation at the fossil site. C?evirme (Erzurum Province, Tekman
district) according to Sickenberg (1975).
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C. umbla, C. baliki, C. damascina, C. buhsei
all Capoeta species
C. sevangi, C. capoeta, C. sieboldii, C.trutta, C. sp.
C. umbla, C. baliki, C. damascina
C. sevangi, C. capoeta
Not identified (tooth genus)
BGR C?ev?rme 1
BGR C?ev?rme 2
BGR C?ev?rme 155?194
BGR C?ev?rme 24?154
BGR C?ev?rme 195?226
BGR C?ev?rme 226?235
BGR C?ev?rme 4?22
BGR C?ev?rme 23
BGR C?ev?rme 3
BGR C?ev?rme 237
BGR C?ev?rme 238?247
Naturmuseum Frankfurt (SMF) and National Museum of Natural Sciences of Madrid
(MNCN) (Table 2). Both fossil and extant specimens publicly deposited in the
above-mentioned collections and accessible by others in a permanent repository.
Identification of isolated fossil pharyngeal teeth
This study uses methodology and terminology established by Ayvazyan et al. (2018). The
isolated fossil pharyngeal teeth are described and identified based on the established
non-overlapping shape characters (??) and shape classes (A to R). Ayvazyan et al. (2018) applied an
artificial (virtual) wear experiment in 3D software to check the possible effects of wear degree
on the teeth morphology, its influence on the transverse cross section and other recorded
characters (e.g. folded edge of grinding surface). The experiment shows that there is no any
significant changes of transverse cross section during applied virtual wearing, while folds of the
grinding surface can change during the wearing process: they deepen, enlarge, or disappear.
Thus, these variable characters are not included in the description of the isolated fossil
pharyngeal teeth. Examples of applied shape characters to identify shape classes are shown on Fig 6.
The identified shape classes within the isolated fossil pharyngeal teeth are applied to identify
the teeth according to the identification key (see S6 Fig in [
Nomenclature issues of isolated pharyngeal teeth of cyprinids
It is always an issue between molecular and morphologic studies regarding the nomenclature
of taxa. This is further complicated if the material is composed by isolated pharyngeal teeth,
thus restricting morphologic observations. To account for this uncertainty we prefer to use the
open nomenclature system for fossil isolated cyprinid teeth.
No permits were required for the described study, which complied with all relevant
Clade Teleostei Mu?ller 1846
Family Cyprinidae Rafinesque, 1810
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Fig 5. Isolated fossil pharyngeal teeth from the early Pliocene locality C?ev?rme (Erzurum Province, Tekman district). (a-e), species/clade diagnostic shape
classes: a, shape class "A" characteristic of C. umbla (BGR C? ev?rme 1). (b), shape class "R", characteristic of C. sieboldi (BGR C?ev?rme 3). (c-d), shape class "J",
characteristic of C. baliki (BGR C?ev?rme 4, 5). (e), clade diagnostic shape class "M", characteristic of Aralo-Caspian clade of genus Capoeta (C. sevangi and C. capoeta)
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BGR C?ev?rme 23). (f-k), genus diagnostic shape class "C" (BGR C?ev?rme 24, 25, 26, 27, 28, 29). (l-s), common shape classes shared by different species. (l-n), shape
class "B" (BGR C?ev?rme 155, 156, 157). (o-q), shape class "F" (BGR C?ev?rme 195, 196, 197). (r-s), shape class "H" (BGR C?ev?rme 226, 227). (t), not identified, possibly
tooth pathology (BGR C?ev?rme 237). (u), not identified (BGR C?ev?rme 238).
Subfamily Barbinae Bleeker, 1859
Genus Capoeta Valenciennes, 1842
Material: 247 isolated fossil pharyngeal teeth collected from the C? evirme (Erzurum
Province, Tekman district) locality (BGR C? ev?rme 1?247).
The studied isolated fossil pharyngeal teeth contain different tooth morphologies. They
include eight main shape classes: "A", "B", "C", "F", "J" "H", "M" and "R" (details about shape
classes see Ayvazyan et al. 2018).
Shape class "C" (Table 1, Fig 5F?5K) (n = 131)?the teeth are spatulate, the tooth body
sharply widens distally. The foot-crown border is not well distinguished, and the foot is nearly
two times narrower than the tooth crown. The teeth are characterized by a relatively narrow
grinding surface, which reminds a hook. Some samples within the isolated fossil pharyngeal
teeth can be identified as replacement teeth based on the presence of resorption traces (Fig 5I?
Shape class "B" (Table 1, Fig 5L?5N) (n = 40)?the tooth body is spatulate, it is widens
distally and the foot is narrower than the crown. The foot-crown border is not well distinguished.
The grinding surface is comma-shaped and wider than the ones among the shape class "C".
Besides this, these teeth have a deep groove on the grinding surface.
Shape class "F" (Table 1, Fig 5O?5Q) (n = 32)?these teeth are also spatulate in shape, the
foot-crown border is not well distinguished. The grinding surface is reniform. In some
specimens the edge of the grinding surface bears some hooks. Within this shape class, also
replacement teeth are recorded (Fig 5P).
Shape class "J" (Table 1, Fig 5C and 5D) (n = 20)?is represented only by replacement teeth,
despite this, the teeth morphology is clearly described by the shape characters ?11 and ?9. The
crown is short, robust and convex posteriorly. A well-developed fold is present at the anterior
Number of samples
(n = )
11 / 21
Fig 6. Examples to describe the isolated pharyngeal teeth based on the shape characters and shape classes. (a), shape class "M", b2 tooth of extant C. capoeta. (b),
shape characters (?5?4) defining shape class "M". (c), shape class "D", a2 tooth of extant C. sieboldi. (d), shape characters (?4?7) defining shape class "D". Details of
shape characters ? and ? see Ayvazyan et al. 2018. The scales are not given to avoid scaling up of the figures.
part of the crown, which slightly divides it into two unequal parts. The grinding surface is
ovate, but broad posteriorly.
Shape class "H" (Table 1, Fig 5R and 5S) (n = 9)?the teeth are molariform. The tooth body
is compressed at the foot-crown border where it bends anteriorly. Due to this, the foot-crown
border is well distinguished. The foot is longer than the crown but has nearly the same width
as the crown. The crown is convex posteriorly. The grinding surface is triangular and possesses
a visible groove.
Shape class "A" (Table 1, Fig 5A) (n = 2)?the tooth is oblong and widens slightly distally.
The tooth body bends anteriorly at the foot-crown border. The tooth body is compressed and
the foot-crown border well distinguished. The crown is slightly convex posteriorly. The
grinding surface is triangular in shape with well visible groove on it.
Shape class "M" (Table 1, Fig 5E) (n = 1)?the tooth body is linear, the foot is shorter than
the crown, but they have the same width along the tooth body. The tooth body bends laterally
at the foot-crown border. The grinding surface is narrow and reniform.
Shape class "R" (Table 1, Fig 5B) (n = 1)?the tooth is molariform. The tooth body is
compressed at the foot-crown border where it bends posteriorly. The foot and crown have nearly
the same length, but the crown is wider than the foot. The grinding surface is reniform and
possesses a deep groove.
An isolated fossil pharyngeal tooth (Table 1, Fig 5T) (n = 1) is not possible to attribute to
one of delineated shape classes. We described this tooth as pathologic as the tooth crown
bends extremely anteriorly, and we assume that this tooth possibly cannot participate in food
The other recorded shape class (Table 1, Fig 5U) (n = 10) is represented only by
replacement teeth and not found within recoded shape classes according to Ayvazyan et al. 2018. We
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marked these teeth as not identified. The crown is convex posteriorly and concave anteriorly.
The grinding surface is half-moon in shape. These teeth are replacement teeth, based on their
morphology we can assume, that they belong to the first teeth row and tooth position a2.
As it is shown in our previous study [
], tooth shape classes can be used for the
identification of isolated pharyngeal teeth at generic and specific levels. Within studied fossil material,
both genus and species diagnostic shape classes are present.
The shape class "C" (tooth position a3-a5) is identified by Ayvazyan et al. 2018 as the only
genus diagnostic shape class for the genus Capoeta. Three shape classes in the studied samples
(?A?, ?J?, ?R?) are considered species diagnostic. These shape classes occur in the first tooth
row at tooth position a2 in extant C. umbla, C. baliki and C. sieboldi respectively. Four other
recorded shape classes "B", "F", "H" and ?M? occur in more than one species. Shape class "M" is
clade diagnostic for both species of the Aralo-Caspian clade C. capoeta and C. sevangi. Finally,
shape classes "B" and "H" are diagnostic for the four species of the Anatolian-Iranian clade or
damascina complex (C. saadii, C. buhsei, C. damascina, C. umbla and C. baliki) [
]. The shape
class ?F? is characteristic of C. trutta, C. sieboldi, C. capoeta and C. sevangi.
Percental distribution of the shape classes of the pharyngeal teeth
The distribution of the shape classes at the pharyngeal bone confines to a certain topology (S5
Fig in [
]). In order to be able to compare the studied fossils with recent teeth (overall 84 teeth
from ten Capoeta species) and/or to estimate the number of potential species present in the
material, the percental distribution of the shape classes within ten recent Capoeta species is
calculated and compared with those in the fossil material [
In the recent species, the species diagnostic shape classes "A", "J" and "R", mainly occur in
the first tooth row at the a2 position (except C. sieboldi which has also diagnostic shape class at
the tooth position b1 [which is also included into percental estimation]), are rare and represent
3% out of 84 pharyngeal teeth of the ten recent species. The genus diagnostic shape class "C"
(tooth positions a3-a5) builds 27% within the studied 84 pharyngeal teeth. The shape classes
"C" and "B" (at the tooth positions a3-a5) make nearly 33% (S4 Fig in [
In the fossil material, the shape class "C" can be referred to around 53% of all teeth; the
shape classes "C" and "B" (a3-a5 positions) make 69%, whereas the species diagnostic shape
classes "A", "J" and "R" (a2 tooth position) comprise 10% of studied isolated fossil pharyngeal
teeth (S1 and S2 Figs).
Morphological observations of isolated fossil pharyngeal teeth revealed, besides the main
distinguished characters (lateral outline (?) and transverse cross-section (?)), further charcters
commonly occuring within both recent and fossil Capoeta. They are "ruptures" of the grinding
surface and the crenated edge of the grinding surface, which are variable and depending on
the degree of tooth wearing (Fig 7) (details see Ayvazyan et al., 2018). These structures are not
considered as a species characteristic.
In our fossil samples, we record eight shape classes where the genus diagnostic shape class ?C?
dominates the assemblage (53%). Identified shape classes as species or clade diagnostic (A, J,
R, M) compose 10% of the assemblage (S1 Fig).
Possible influence of plasticity and allometry on high diversity of recorded
The literature provides examples of the potential effects of plasticity on the dentary bone and
tooth morphology mainly in cichlid fish cultures by applying contrasting diets (soft and hard)
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Fig 7. Additional morphological characters (besides the shape characters (??) in fossil and extant pharyngeal teeth (not to scale). (a), Capoeta sp., b3 tooth (extant)
(SAPM-PI-00719, SNSB). (b), C. trutta, a5 tooth (extant) (SAPM-PI-02908, SNSB). (c-d), isolated fossil pharyngeal teeth (identified as shape class "C" and "F" respectively)
(BGR 6, 16). (e), isolated fossil pharyngeal tooth (BGR 5). (f), C. capoeta, b2 tooth (extant) (GPIT-OS-00860a), both are identified as shape class "M". The ruptures of
grinding surface are marked by red arrows (a, b, c, d) and an example of very similar tooth morphology in fossil (e) and extant (f) isolated pharyngeal teeth.
]. These studies recorded some degree of phenotypic plasticity of dentary bone
morphology and in some cases tooth size. The influence of these two diets on the development of
the cyprinid pharyngeal dentition is also tested in the benthophagous cyprinid black carp.
Dietary did not change the tooth morphology, but, instead, it has been found that broad diet may
influence the frequency of tooth replacement and size patterns . These studies are mainly
based on aquarium experiments in benthophagous species where two extreme diets
(commercial fish as a soft and snails as hard food) are tested. Under natural conditions, fishes are not
forced to feed on only one type of food. Thus, it is data can be applied to, in the present paper
studied algae-scrapping species Capoeta, which are recorded from single geological layer and
are sympatric individuals in a uniform environment. Considering this, the effect of feeding on
different food should not be considered biasing on the carp pharyngeal tooth morphology,
and, thus, we exclude the effect of plasticity on the studied fossil material.
Allometric shifts in pharyngeal tooth morphology cannot explain the high diversity of
recorded shape classes in the studied fossil samples. Morphological shape remodeling in
cyprinids happens in very early stages of their ontogeny. Juveniles (standard size of a few mm) have
different tooth morphology than the adult samples, but the significant morphological changes
are finalized in this early stage. Thus, the adult dentition in cyprinid fishes is completed by at
the later larvae or juvenile stages [
]. Our fossil material is represented by adult individulas,
as the studied fossil pharyngeal teeth sizes vary between 0.8?3 mm (it is a sampling artifact
introduced by mesh size limitation washing collection technique). Therefore, our fossil
samples is composed of isolated pharyngeal teeth of adult individuals.
For species-level taxonomy we discuss two possible interpretations. The assemblage can be
interpreted to document either a single, very heterodont species or several Capoeta species.
1. The fossil assemblage documents one species. The recent Capoeta species are
characterized by different degree of heterodonty, which varies between three and six shape classes
per species. For instance, C. damascina, the most heterodont extant species, is characterized by
six different shape classes [
]. The second most heterodont species C. umbla (Heckel, 1843) is
characterized by five different shape classes, four of them are shared with C. damascina. Eight
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shape classes, as found in our fossil samples, is unprecedented among extant species. It is also
highly unlikely that a fossil species shows this degree of heterodonty, given the ten tooth
positions at pharyngeal bones are present. Therefore, we consider the ?single species? interpretation
as rather unlikely.
2. The fossil assemblage represents more than one species. The specific identification of
extant Capoeta species is possible only on the morphology of the teeth at the tooth position a2
]. The C? ev?rme association contains four shape classes, which are species-specific among
recent taxa at the a2 position: the shape class ?A? characterizes C. umbla, the shape class ?J? is
typical for C. baliki (both species belong to the Anatolian-Iranian clade) and the shape class
?R? is found only in C. sieboldi (sieboldi clade). The shape class ?M? is shared at the a2 position
by two closely related Aralo-Caspian species C. capoeta and C. sevangi. Therefore, we assume
that the C? ev?rme assemblage is constituted of four species.
The four discussed extant species are also characterized by other shape classes, which are
not found within the studied fossil material. The shape class ?I? is common in C. umbla and C.
baliki, it occurs at the topological positions b2, b3 and c2. These teeth are small and may not
be found due to taphonomic or sampling bias (tooth diameter is smaller than 0.8 mm). Two
additional shape classes ?N? and ?O?, which are missing in our sample, characterize the two
Aralo-Caspian Capoeta species Capoeta sevangi and Capoeta capoeta, at the tooth position a2.
We interpret the lack of these species characteristic shape classes by younger divergence of
these species (see below).
Our results indicate the presence of possible four species in the fossil assemblage, which
belong to three different clades (Anatolian-Iranian, Aralo-Caspian, and sieboldi clades) of the
genus Capoeta. According to all molecular studies [
29, 56, 57
], these three clades are
monophyletic and sister groups to the Mesopotamian clade (Fig 3a).
The evolution of the genus Capoeta as a species flock scenario
Greenwood (1984) suggests that, in order to identify a group of organisms as species flock, the
representatives should be monophyletic and endemic to an area they inhabiting [
]. Later on,
five main criteria are distinguished to detect the flock species [
]: 1) monophyly, 2) high
species diversity (speciosity), 3) high level of endemism, 4) morphological and ecological
diversity; and 5) habitat dominance in terms of biomass. A later study , suggests to
concentrate on three robust, easier to determine criteria such as monophyly, endemism and
speciosity. This study suggests ranking the ecological criterion as secondary. Our fossil Capoeta
samples correspond to all five criteria sensu Eastman and McCune (2000) and can thus be
regarded as a species flock. The extant Capoeta is a monophyletic phytophagous barbin genus,
widely distributed in West Asian and the Ponto-Caspian water basins and comprise 30 extant
5, 29, 35, 56
]. Our four fossil species (Capoeta cf. umbla, C. cf. baliki, C. cf. sieboldi, C.
sp. capoeta/sevangi) belong to a monophyletic clade composed of Capoeta sieboldi,
AnatolianIranian and Aralo-Caspian species (Fig 3A) endemic to the drainage systems of the Black and
Caspian seas and Persian Gulf (Fig 2), thus, fulfilling the three main criteria for species flock
recognition . Certainly, we cannot be fully definite that our fossil taxa are also
monophyletic. However, considering that the phylogenetic analysis using the morphology of extant
pharyngeal teeth [
] placed the species in the same topology as the molecular phylogenetic
analysis, we are confident that the fossil species attribution correspond to extant taxa.
Nevertheless, as in every biological study species identification retain certain degree of uncertainty,
which would potentially affect the probable monophyly of the fossil taxa.
The endemic occurrence of the genus Capoeta in Western Asia and the Ponto-Caspian
region is supported by its exclusive extant and fossil record in the region [
7, 30, 60?62
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taxonomic studies of this genus show the morphological and meristic diversity of the extant
Capoeta species [
9, 39, 63?65
], but detailed ecologic studies are lacking so far. The fifth criteria
(habitat dominance in terms of biomass) is more difficult to access for the fossil
palaeocommunity. However, within the studied samples from the locality C? ev?rme Capoeta dominates not
only by the species richness over Leuciscus (one undetermined medium-size species), but also
in terms of numbers of specimens (247 Capoeta teeth versus 41 Leuciscus teeth), suggesting
habitat dominance of Capoeta in the Tekman Palaeolake of the I??klar Formation 4 Ma ago.
Our results are largely in agreement with estimated divergence times within Capoeta [
showing that at 4 Ma C. sieboldi is already diverged and the Aralo-Caspian clade species C.
capoeta and C. sevangi are not yet separated, which explains the lack of their species-specific
tooth shape classes "N" and "O". The fossil Aralo-Caspian clade taxon may, therefore, represent
a newundescribed species ancestral to the extant members of this clade. However, published
divergence times seem to be overestimated since the fossil calibration points used for the
molecular clock are too old, maybe by a factor of two Barbus sp. set at 18 Ma citing Bo?hme &
Ilg 2003 refer in fact to Barbus s. l., which is probably closer related to Cyprinion; the oldest
Barbus s. s. fossils are known from sediments of age at least 8 Ma, Bo?hme unpublished data)
]. Nevertheless, the oldest unequivocal Luciobarbus with affinities to L. subquincunciatus
(the sister clade of Capoeta, Fig 3A and 3B) is L. vindobonensis from 9.8 Ma old deposits in
], suggesting that the evolution of Capoeta is largely a late Miocene event.
The presence of a four-million-year old Capoeta species flock in the Tekman Basin with
members of three recent clades is very remarkable. We hypothesize, that the Tekman
Palaeolake, which was part of a large Armenian Highland lake system, was a place of the speciation of
Capoeta species related to the three recent clades of the genus (Anatolian-Iranian,
Aralo-Caspian and sieboldi). Moreover, the huge Armenian Highland lake system, which formed during
the late Miocene and represents the source of all major rivers in Western Asia and the
PontoCaspian region where Capoeta is widely distributed, could represent the centre of origin of
Capoeta including its Mesopotamian clade.
A recent study shows that tectonic reorganization in the region, starting about the
Miocene-Pliocene transition (ca. 5.5 Ma) along the East and North Anatolian faults [
resulted in substantial surface uplift and probably caused the gradual reshaping of the
hydrological network in the area. This could largely contribute to dispersal and further speciation of
the members of the species flock into their distribution areas nowadays.
The possible species flock scenario of the genus Capoeta as well as the reorganization of the
palaeolake system in Armenian Highland are hypothetically illustrated in Fig 8, where three
main stages of lake evolution.
The other possible explanation of our results could be the concept of secondary contact.
This scenario (speciation of hybrids) is very similar to the above suggested species flock model,
however, without any genetic information we cannot be precise about this hypothesis. More
studies and more fossil sites inside and outside distribution area of Capoeta are needed to test
our hypothesis, but according to the current available data, the fossil species flock
interpretation is the most plausible.
For the first time, a detailed study of the isolated fossil pharyngeal teeth of the genus Capoeta
(n = 247) is provided. The description and identification of the fossil material from C? ev?rme
(Erzurum Province, Tekman district) is based on the methodology introduced by Ayvazyan
et al. 2018. We show that our methodology is applicable to the fossil record of the genus
Capoeta and allows identification of the isolated fossil pharyngeal teeth at species level. Within
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Fig 8. Hypothetical evolutionary stages of the palaeolake system of Armenian Highland since latest Miocene. Three main stages are suggested (marked by
blueish colours): formation, maximum of lake expansion, decay and fully development of present-day drainage system. The monophyletic clade of recorded
species within the fossil material shows the presence of the species flock of Capoeta at 4 Ma ago in palaeolake system of Armenian Highland.
the studied fossil material eight shape classes are distinguished, four of them are species or
clade diagnostic and indicate the presence of the four sympatric Capoeta species (C. cf. sieboldi,
C. cf. umbla, C. cf. baliki and C. sp. capoeta/sevangi) in the Tekman Palaeolake at 4 Ma. These
four species belong to a monophyletic clade of the genus and today they are distributed in
different water basins (Euphrates/Kura/Black Sea) of Western and Ponto-Caspian region. We
interpret this high local diversity of closely related species in terms of the species-flock model.
Literature review suggests that the Tekman Palaeolake was part of an unrecognized huge
late Miocene to Pliocene palaeolake system in the present-day Armenian Highland and we
hypothesized that the evolution of Capoeta occurred there during the late Miocene. Pliocene
tectonic activities disrupted this lake system and resulted in the very characteristic
biogeographic distribution of Capoeta in West Asian and Ponto-Caspian drainage systems today.
S1 Fig. Frequency distribution of recorded shape classes in the C? ev?rme sample (n = 247).
S2 Fig. The frequency (in % of all studied teeth, n = 247) of the tooth positions for isolated
fossil pharyngeal teeth from C? ev?rme.
S1 Table. The distribution of the extant ten Capoeta species, used for comparison.
We would like to thank H. Schulz (Tu?bingen) for assistance with the SEM at the laboratory of
the University of Tu?bingen, Prof. Samvel Pipoyan for fruitful discussions regarding recent
Capoeta species. We thank to Dr. Henriette Obermaier from the Bavarian State Collection for
Anthropology and Palaeoanatomy for an access to the osteological collection, Munich (SNSB),
Fabian Herder and Nisreen Alwan Senckenberg Naturmuseum Frankfurt (SMF). The first
author gratefully thanks to Prof. Dr. I. Doadrio and his working group for hosting in Madrid
and for an access to the ichthyological collection, National Museum of Natural Sciences of
17 / 21
Conceptualization: Davit Vasilyan, Madelaine Bo?hme.
Data curation: Anna Ayvazyan, Davit Vasilyan, Madelaine Bo?hme.
Formal analysis: Anna Ayvazyan.
Funding acquisition: Madelaine Bo?hme.
Investigation: Anna Ayvazyan, Davit Vasilyan, Madelaine Bo?hme.
Methodology: Anna Ayvazyan, Madelaine Bo?hme.
Supervision: Davit Vasilyan, Madelaine Bo?hme.
Validation: Anna Ayvazyan, Davit Vasilyan, Madelaine Bo?hme.
Visualization: Anna Ayvazyan.
Writing ? original draft: Anna Ayvazyan.
Writing ? review & editing: Davit Vasilyan, Madelaine Bo?hme.
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