Research Article |
Corresponding author: Ekaterina Vasil`eva ( vas_katerina@mail.ru ) Academic editor: Jan Kotusz
© 2022 Victor Vasil`ev, Ekaterina Vasil`eva.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Vasil`ev V, Vasil`eva E (2022) Triploid forms’ karyotypes of spined loaches from the genus Cobitis (Actinopterygii: Cypriniformes: Cobitidae) of the upper Dnieper and Western Dvina rivers: Analysis of the triploids’ origin. Acta Ichthyologica et Piscatoria 52(1): 67-75. https://doi.org/10.3897/aiep.52.81191
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Unisexual forms of lower vertebrates (fish, amphibians, and reptiles) reproduced by parthenogenesis, gynogenesis, or hybridogenesis are represented by diploids, triploids, or tetraploids, whose origin is associated with interspecific hybridization. Among fish species, the highest variability of unisexual polyploids was found in the genus Cobitis. The structure of their genomes and putative parental species holds great interest for the investigation in association with questions about possible evolutionary success. In particular, it serves to elucidate the possible high colonization properties of a few polyploid forms, in contrast to the local history of rather numerous hybrid forms with a limited distribution. Therefore, the aim of this study was to describe the karyotype structure of two newly discovered triploid forms of the genus Cobitis, to analyze their origin and putative parental species. The karyotype structure of 182 spined loach individuals from the Western Dvina River and 91 individuals from the upper Dnieper River of the Smolensk District of Russia was studied. A total of 121 studied individuals from the Western Dvina comprised triploid females with a chromosome number 74 and karyotype consisting of 13 meta-, 39 submeta-, and 22 subtelo-acrocentric chromosomes. Among loaches collected in the upper Dnieper River, 42 triploid females were found with 74 chromosome number including 23 meta-, 26 submeta-, and 25 subtelo-acrocentric chromosomes. Other individuals from both localities were karyologically identified as Cobitis taenia Linnaeus, 1758 with 2n = 48. The triploid form of spined loaches of the Western Dvina River most likely arose as a result of the hybridization of Cobitis tanaitica Bǎcescu et Mayer, 1969 and C. taenia. The range of C. tanaitica, whose karyotype is characterized by an evolutionarily fixed Y-autosomal translocation, is limited to the rivers of the northern coast of the Black Sea. Therefore, hybridization probably happened in late Pleistocene in the Dnieper River system, where both parental species occur. The triploid form that arose here is unique for the Baltic Sea basin. Probably, it colonized the Western Dvina through the artificial Berezinskaya water system (Berezina Canal = Daugava–Dnieper Canal), but at the same time it was forced out of its area of origin by other triploid forms which are now widespread there. According to the karyotype structure, the triploid form, common for both the upper and lower reaches of the Dnieper, has a trihybrid origin, with probable hybridization of Cobitis elongatoides Bǎcescu et Mayer, 1969, C. tanaitica, and yet unidentified species Cobitis sp. Both studied triploid forms are parts of unisexual-bisexual complexes, in which their putative diploid maternal species (C. tanaitica and C. elongatoides) are absent, and the role of the host species involved in reproduction belongs to C. taenia.
hybrid origin, parental diploid species, polyploidy, unisexual-bisexual complexes
About 90 unisexual forms reproducing by parthenogenesis, gynogenesis, or hybridogenesis are known among fish, amphibians, and reptiles at present. These forms can be diploid, triploid, and tetraploid; however triploid unisexual forms are much more widespread, while tetraploids are extremely rare. The genesis of unisexual forms is associated with interspecific hybridization, while triploid and tetraploid forms can have not only dihybrid, but even trihybrid origin (see
In contrast to parthenogenesis in several reptiles (see
The first clonal-bisexual (diploid-polyploid) complex in the genus Cobitis was noted in 1981 in the Volga River basin (
In this study, we describe the karyotypes of two triploid forms found in the Western Dvina and Upper Dnieper rivers, respectively, and analyze their origin and putative parental species.
Materials for karyological research were collected in June 2003 and June 2005 in the Western Dvina River (vel Zapadnaya Dvina vel Daugava) at Velizh City, Smolensk District of Russia, 55°36′N, 031°12′E, and in June 2003 and June 2005 in the Upper Dnieper at Bilino village, Smolensk District of Russia, 55°13.4′N, 033°28.7′E (Fig.
Among the karyotyped spined loaches of the Western Dvina River, 44 (63.8%) were identified as triploid females in the sample collected in 2003 and 77 (68.1%)—in the sample collected in 2005. These triploids had 74 chromosomes, including 13 meta-, 39 submeta- and 22 subtelo- and acrocentrics (Table
The karyotype structure of the studied triploid forms, their putative parental diploid species of Cobitis and diploid species coexisting with triploids.
River system | Chromosome number | m | sm | sta | Putative parent species | Coexisting diploid species |
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Western Dvina | 74 | 13 | 39 | 22 | 2 C. tanaitica–C. taenia | C. taenia |
Upper Dnieper | 74 | 23 | 26 | 25 | C. elongatoides–C. tanaitica–Cobitis sp. | C. taenia |
The karyotype structure of diploid spined loach species of the genus Cobitis apparently participated in the origin of polyploid forms.
Species | River system | Chromosome number | m | sm | sta | Reference |
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C. taenia | Volga, Dnieper, Dniester, south Bug, Elbe, Weser, Vistula, Odra | 48 | 10 | 18 | 20 |
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C. taenia | Odra | 48 | 10 | 20 | 18 |
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C. taenia | Vistula | 48 | 12 | 18 | 18 |
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C. elongatoides | Elbe, Danube, Odra, Tisza | 50 | 30 | 16 | 4 |
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C. elongatoides | Odra | 50 | 28 | 18 | 4 |
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C. elongatoides | Danube, Kamchya, Elbe, Odra | 50 | 22 | 26 | 2 |
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C. tanaitica, females | Dnieper estuary | 50 | 8 | 24 | 18 |
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C. tanaitica, males | 49 | 9 | 24 | 16 | ||
C. tanaitica, females | Don, Dnieper, Dniester, Kuban | 50 | 8 | 28 | 14 |
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C. tanaitica, males | 49 | 9 | 28 | 12 | ||
C. tanaitica A p. 395 | Danube, Odra, Sinoe, Don | 50 | 10 | 24 | 16 |
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C. tanaitica
A Fig. |
50 | 10 | 26 | 14 | ||
C. tanaitica A | Danube, Sinoe | 50 | 10 | 26 | 14 |
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C. tanaitica A | Danube | 50 | 10 | 22 | 18 |
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C. taurica | Crimea | 50 | 10 | 30 | 10 |
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C. pontica | Veleka | 50 | 10 | 30 | 10 |
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C. taurica A | Crimea, S. Bug, Veleka | 50 | 10 | 30 | 10 |
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C. melanoleuca | Volga | 50 | 8 | 18 | 24 |
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C. strumicae | Kamchya, Jantra | 50 | 10 | 20 | 20 |
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Karyotype of triploid form of the genus Cobitis from the Western Dvina River (A) and haploid sets of the putative parental species involved: B, C. taenia; C, C. tanaitica, female; D, C. tanaitica, male; m = metacentric, sm = submetacentric, st = subtelocentric, a = acrocentric chromosomes.
Triploid form in the Western Dvina basin. According to the number of chromosomes (Fig.
In this line, it is necessary to discuss the differences observed in the structure of the karyotype of C. tanaitica in our studies and in publications of other authors (
Among the described triploid karyotypes, the fishes of the Western Dvina are most similar to the fishes of the Oława (Odra River system) and Bug (Vistula River system) rivers. They also have 3n = 74 with a low number of metacentric and a high number of submetacentric chromosomes (Table
The karyotype structure of previously studied triploid forms, their putative parental diploid species of Cobitis (as identified in the cited publication) and diploid species coexisting with triploids.
River system | Chromosome number | m | sm | sta | Putative haploid sets of parental species | Coexisting diploid species | Reference |
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Odra (Oława) | 74 | 16 | 36 | 22 | 2 Cobitis sp. (2n = 49)–Cobitis sp. 1 (2n = 50) | 2n = 49 (19 m + 18 sm + 12 sta) |
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Vistula, Bug | 74 | 18 | 33 | 23 | C. taenia–2 Cobitis sp. (2n = 50, 12 m + 24 sm + 14 sta) | C. taenia |
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Lower Dnieper | 74 | 23 | 25 | 26 | C. taenia–2 Cobitis sp. | C. tanaitica A |
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Volga | 74 | 23 | 27 | 24 | C. taenia–2 Cobitis sp. or C. taenia–C. tanaitica–Cobitis sp. 1 or C. taenia–C. elongatoides–Cobitis sp. 2 | C. taenia, C. melanoleuca |
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Vistula, Odra | 73 | 24 | 27 | 22 | 2 C. taenia–C. elongatoides | C. taenia | |
Odra (Polska Woda) | 74 | 24 | 36 | 14 | 2 C. elongatoides–C. taenia | C. elongatoides AA |
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Vistula, Odra | 74 | 21 | 31 | 22 | C. taenia–2 Cobitis sp. | C. taenia, C. taenia × C. elongatoides |
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Elbe (Pšovka creek) | 74 | 35 | 25 | 14 | 2 C. elongatoides–C. taenia | C. elongatoides, C. taenia |
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Odra | 74 | 33 | 27 | 14 | C. taenia–2 C. elongatoides | C. elongatoides | |
Danube (Dyje River) | 75 | 38 | 29 | 8 | 2 C. elongatoides–Cobitis sp.1 | C. elongatoides |
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Tisza basin | 75 | 35 | 27 | 13 | 2 C. elongatoides–C. tanaitica | C. elongatoides |
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Odra (Polska Woda) | 75 | 24 | 36 | 15 | 2 C. elongatoides–C. taenia or Cobitis sp. | C. elongatoides |
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Odra (Polska Woda) | 75 | 24 | 35 | 16 | 2 C. elongatoides–C. taenia or Cobitis sp. | C. elongatoides |
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Thus, the triploid form of the Western Dvina differs from other triploids found in the Baltic Sea basin (Odra, Vistula) by the karyotype structure and the supposed origin; this form also differs from other triploids revealed in various European river systems (Table
It is well known that the recent freshwater fish fauna of the Baltic Sea is one of the youngest. The Baltic Sea depression was covered with ice during the last glacial advance in the Pleistocene and was filled with fresh water at the end of the Quaternary after the retreat of the ice sheet, starting about 13 thousand years ago (
Triploid form in the upper Dnieper. The karyotype structure of triploid females in the upper Dnieper basin indicates its trihybrid origin (Fig.
According to the second hypothesis of the origin of triploids from the Dnieper, the parental diploid with 24 chromosomes in the haploid set may be a male of C. tanaitica. After removing its haploid set (Fig.
The triploid form of spined loaches of the Western Dvina River most likely arose as a result of the hybridization of Cobitis tanaitica and C. taenia. Since the range of C. tanaitica, whose karyotype is characterized by an evolutionarily fixed Y-autosomal translocation, locally distributed in the rivers of the northern coast of the Black Sea, hybridization probably happened in the Dnieper River system, where both parental species occur. The triploid form that arose here, unique for the Baltic Sea basin, probably colonized the Western Dvina through the artificial Berezinskaya water system (Berezina Canal), but at the same time it was forced out of its area of origin. According to the karyotype structure, the triploid form, common both in the upper and lower reaches of the Dnieper, has a trihybrid origin, with probable hybridization of C. elongatoides, C. tanaitica and an unknown species Cobitis sp. Both studied triploid forms are parts of unisexual-bisexual complexes, in which their putative diploid maternal species (C. tanaitica and C. elongatoides) are absent, and the role of the host species involved in reproduction belongs to C. taenia. This phenomenon can be explained by the strong ecological competition of the unisexual form and its maternal species, as well as the deep northward dispersion observed for the triploid forms of the Western Dvina and upper Dnieper basins, where maternal species cannot exist due to their more southerly origin.
The authors are deeply grateful to an anonymous reviewer for the analysis of the work and helpful comments. Scientific investigations of EV are supported by the State Project of ZMMU # 121032300105-0.