Content uploaded by Spartak Litvinchuk
Author content
All content in this area was uploaded by Spartak Litvinchuk
Content may be subject to copyright.
A preview of the PDF is not available
Mass polyploidy in Rana esculenta hybridogenic complex (Ranidae, Anura, Amphibia) in eastern Ukraine
Abstract
Mass triploidy in hybrid Rana esculenta was revealed by means of DNA flow cytometry
in 19 localities of eastern Ukraine (Kharkov, Donetsk, and Lugansk provinces). Triploids
consist of two groups in terms of parental species genomes: LLR and LRR. The both
groups were recorded in population systems of the E and R–E types. Two tetraploids
were found as well. All polyploids were distributed along the middle part of Seversky
Donets River basin (above 450 km). The nearest localities with mass occurrence of
triploidy were known at distance of 1000 km (Poland) or 1500 km (Hungary).
... Also in one known case an LLR female produced both diploid and haploid gametes at the same time (Christiansen 2009). About 10 years ago mass polyploidy in P. esculentus was discovered in the middle stretch of the Seversky (=Siverskyi) Donets River (Borkin et al. 2004Borkin et al. , 2005Borkin et al. , 2006). This territory proved to be unique in terms of quite diverse population systems and was named the Seversky Donets centre of genetic diversity of green frogs (Shabanov and Litvinchuk 2010; Dedukh et al. 2015). ...
... Moreover, recently it was found that R and L genomes in hybrids from the centre may represent independent evolutionary lineages (Hoffmann et al. 2015 ). Here, we found RR populations , and various types of population systems containing hybrids (Borkin et al. 2004Borkin et al. , 2005Borkin et al. , 2006 Korshunov 2010). Triploid P. esculentus frogs are distributed along the Seversky Donets River over an area over 480 km in length in Kharkiv, Donetsk and Luhansk oblasts of Ukraine and in Rostov Oblast of Russia. ...
... Therefore, the suggestion mentioned above concerning the role of triploid males would be incorrect, and production of L gametes can be maintained predominantly by diploid hybrids. In north-eastern Ukraine, triploid hybrids usually coexist with diploid P. esculentus and P. ridibundus and, rarely, with diploid P. esculentus only in pure hybrid HPS (Borkin et al. 2004Borkin et al. , 2005 Korshunov 2010 ). Our data, concerning genome composition of sperm in triploid males, demonstrated that such males produced haploid gametes only and lacked diploid sperm (Table 1). ...
Hybridization and polyploidy play an important role in animal speciation. European water frogs of the Pelophylax esculentus complex demonstrate unusual genetic phenomena associated with hybridization, clonality and polyploidy which presumably indicate an initial stage of reticulate speciation. The Seversky Donets River drainage in north-eastern Ukraine is inhabited by both sexes of the diploid and triploid hybrid P. esculentus and only one parental species Pelophylax ridibundus. Based on the presence of various types of hybrids, all populations studied can be divided into three geographical groups: I) P. ridibundus-P. esculentus without triploids; II) P. ridibundus-P. esculentus without diploid hybrids; and III) P. ridibundus-P. esculentus with a mixture of diploids and triploids. A study of gametogenesis revealed that diploid P. esculentus in populations of the first type usually produced haploid gametes of P. ridibundus and a mixture of haploid gametes that carried one or another parental genome (hybrid amphispermy). In populations of the second type, hybrids are derived from crosses of P. ridibundus males with triploid hybrid females producing haploid eggs with a genome of P. lessonae. Therefore, we suggest that clonal genome duplication in these eggs might be the result of suppression of second polar body formation or extra precleavage endoreduplication. In populations of the third type, some diploid females can produce diploid gametes. Fertilization of these eggs with haploid sperm can result in triploid hybrids. Other hybrids here produce haploid gametes with one or another parental genome or their mixture giving rise to new diploid hybrids.
... This hybridogenic species features an unusual meroclonal inheritance, when only a fraction of the inherited genome is clonal (Vinogradov et al., 1990; Plötner, 2005). Many its populations include a considerable fraction of polyploids (Borkin et al., 2004aBorkin et al., , 2005). In addition, a number of species morphologically similar to lake frog were identified using molecular, biochemical , and bioacoustic methods. ...
Heat resistance of the gastrocnemius muscle was studied in five species of the Rana esculenta complex. It was similar in R. bedriagae, R. lessonae, and in the European form of R. ridibunda; while North African R. saharica demonstrated a lower heat resistance. No heterosis was expressed in R. esculenta, a clonal hybrid of R. lessonae and R. ridibunda, for the heat resistance of the muscle. Moreover, this species demonstrated low heat resistance at the highest test temperature
(42°C). Comparison of diploid and triploid R. esculenta syntopically occurring in the same water bodies demonstrated no differences between them, thus, suggesting that polyploidy
has no effect on this parameter at least in this case.
... This hybridogenic species features an unusual meroclonal inheritance, when only a fraction of the inherited genome is clonal (Vinogradov et al., 1990; Plötner, 2005). Many its populations include a considerable fraction of polyploids (Borkin et al., 2004aBorkin et al., , 2005). In addition, a number of species morphologically similar to lake frog were identified using molecular, biochemical , and bioacoustic methods. ...
Heat resistance of the gastrocnemius muscle was studied in five species of the Rana esculenta complex. It was similar in R. bedriagae, R. lessonae, and in the European form of R. ridibunda; while North African R. saharica demonstrated a lower heat resistance. No heterosis was expressed in R. esculenta, a clonal hybrid of R. lessonae and R. ridibunda, for the heat resistance of the muscle. Moreover, this species demonstrated low heat resistance at the highest test temperatures (42 degrees C). Comparison of diploid and triploid R. esculenta syntopically occurring in the same water bodies demonstrated no heat resistances between them, thus, suggesting that polyploidy has no effect on this parameter at least in this case.
The occurrence of three green frog taxa (Pelophylax lessonae, P. ridibundus, and P. esculentus) in Kaliningrad oblast’ of Russia was evidenced by DNA flow cytometry analysis. Almost all frogs were diploid. Only one young specimen of P. esculentus proved to be a triploid with two genomes of P. ridibundus and one genome of P. lessonae. The triploidy occurrence among hybrids was equal to 1.1%. Two species (P. lessonae and P. esculentus) seem to be distributed over all territory of Kaliningrad oblast’. The third species (P. ridibundus) predominantly inhabits the western part of the region, where it can be found in brackish water bodies (4.7 – 6.7%). Six population systems were revealed; with a single species (R, L, and, probably, E) and with mixed species populations (L-E, R-E, and R-E-L). The study of P. esculentus sperm in males taken from the R-E, L-E, and R-E-L systems demonstrated that all of them produced gametes with the ridibundus genome.
The occurrence of three green frog taxa (Pelophylax lessonae, P. ridibundus, and P. esculentus) in Kaliningrad oblast’ of Russia was evidenced by DNA flow cytometry analysis. Almost all frogs were diploid. Only one young specimen of P. esculentus proved to be a triploid with two genomes of P. ridibundus and one genome of P. lessonae. The triploidy occurrence among hybrids was equal to 1.1%. Two species (P. lessonae and P. esculentus) seem to be distributed over all territory of Kaliningrad oblast’. The third species (P. ridibundus) predominantly inhabits the western part of the region, where it can be found in brackish water bodies (4.7 – 6.7‰). Six population systems were revealed; with a single species (R, L, and, probably, E) and with mixed species populations (L-E, R-E, and R-E-L). The study of P. esculentus sperm in males taken from the R-E, L-E, and R-E-L systems demonstrated that all of them produced gametes with the ridibundus genome.
Incompatibilities between parental genomes decrease viability of interspecific hybrids; however , deviations from canonical gametogenesis such as genome endoreplication and elimination can rescue hybrid organisms. To evaluate frequency and regularity of genome elimination and endoreplication during gametogenesis in hybrid animals with different ploi-dy, we examined genome composition in oocytes of di-and triploid hybrid frogs of the Pelo-phylax esculentus complex. Obtained results allowed us to suggest that during oogenesis the endoreplication involves all genomes occurring before the selective genome elimination. We accepted the hypothesis that only elimination of one copied genome occurs pre-meiotically in most of triploid hybrid females. At the same time, we rejected the hypothesis stating that the genome of parental species hybrid frogs co-exist with is always eliminated during oogenesis in diploid hybrids. Diploid hybrid frogs demonstrate an enlarged frequency of deviations in oogenesis comparatively to triploid hybrids. Typical for hybrid frogs deviations in gametogenesis increase variability of produced gametes and provide a mechanism for appearance of different forms of hybrids.
In eastern Ukraine, the Rana esculenta complex consists of three species: R. lessonae, R. ridibunda, and hybrid R. esculenta. The first one was rare, whereas two latter frog taxa were very common. Based on DNA flow cyto-metry, mass occurrence of the triploidy in Rana esculenta has been revealed in 14 localities of Kharkov, Do-netsk, and Lugansk Provinces. One hybrid specimen from Kharkov Province was tetraploid. All polyploids were recorded along the middle part of Seversky Donets River (above 450 km). Triploids comprised two groups with different genome composition (LLR and LRR), and were found in three types of population systems (E, R–E, and L–E–R). Geographic distribution of polyploidy in European green frogs is briefly outlined. Different meth-ods of ploidy level identification are discussed. The chromosome count and nuclear DNA cytometry provide the most reliable data.
Poland is inhabited by the two water frog species Rana ridibunda (genotype RR) and Rana lessonae (LL) and their hybrido-genetic hybrid Rana esculenta. Besides diploid (RL) hybrids two triploid (RRL, RLL) forms were found. In most populations the hybrid occurs syntopically with only one of the parental species. Concerning their genotypic structure water frog populations can be subdivided into three systems: the L-E (lessonae-esculenta) system, the R-E (ridibunda-esculenta) system and the E-E (esculenta-esculenta) system. The composition of water frog populations in Poland is highly differentiated. Among 27 population types described from central Europe 18 types were found in Poland. The highest diversity of population types was seen in the R-E system (8 types). In the L-E system three and in the E-E system four different types were found. Among 11170 investigated adult water frogs 690 (6%) presumptive triploid R. esculenta individuals occurred. In western Poland the proportion of triploid individuals and the diversity of population types was higher (7.7% triploid individuals, 13 population types) than in the eastern parts of the country (0.2% triploid individuals, six population types). The distribution picture of triploid individuals in western Poland is similar to that seen in eastern Germany (as a rule a high proportion of triploids occurs) while in eastern Poland the distribution pattern of triploid genotypes resembles the situation observed in the territory of the former Soviet Union (nearly no triploids appear).
Cytological aspects of hemiclonal (meroclonal) inheritance in diploid and triploid males of the hybridogenetic frog Rana esculenta (Rana ridibunda x Rana lessonae) have been studied by DNA flow cytometry. The fact that the R. ridibunda genome contains 16% more DNA than the R. lessonae genome provides the ability to discern cells containing genomes of any species from the water-frog complex under study. Data are presented showing that elimination of the R. ridibunda genome occurs in hybridogenetic males from certain populations. In triploid males, the cytogenetic mechanism of hemiclonal inheritance is simpler than in diploids: after the elimination of a genome (always the genome in the minority in the triploid set; "homogenizing elimination"), no compensatory duplication of the remaining genetic material is necessary, as it is in diploids. The process of elimination can be visualized in triploid males by using DNA flow cytometry to identify cells in the special phase of the spermatogonial cell cycle that we termed the E phase.
Âèäîîáðàçîâàíèå, ãèáðèäèçàöèÿ è ïîëèïëîèäèÿ ó çåìíîâîäíûõ Ïàëåàðêòèêè // Âîïðîñû ãåðïåòîëîãèè. — Ïóùèíî; Ìîñêâà
- Ë Áîðêèí
Áîðêèí Ë. ß. Âèäîîáðàçîâàíèå, ãèáðèäèçàöèÿ è ïîëèïëîèäèÿ ó çåìíîâîäíûõ
Ïàëåàðêòèêè // Âîïðîñû ãåðïåòîëîãèè. — Ïóùèíî; Ìîñêâà, 2001. — C.
46–48.
Ñåò÷àòîå (ãèáðèäîãåííîå) âèäîîáðàçîâàíèå ó ïîçâîíî÷íûõ
- Ë ß Áîðêèí
- È Ñ Äàðåâñêèé
Áîðêèí Ë. ß., Äàðåâñêèé È. Ñ. Ñåò÷àòîå (ãèáðèäîãåííîå) âèäîîáðàçîâàíèå ó
ïîçâîíî÷íûõ // AEóðí. îáù. áèîë. — 1980. — 41, ¹ 4. — Ñ. 485–506.
A new population system of water frogs discovered in Hungary
- H G Tunner
- S Heppich-Tunner
Tunner H. G., Heppich-Tunner S. A new population system of water frogs discovered in
Hungary // Korsós Z., Kiss I. (eds.), Proceedings of the 6 th Ordinary General
Meeting of the Societas Europaea Herpetologica. 19–23 August 1991. Budapest,
Hungary. — Budapest, 1992. — P. 453–460.
Die Wasserfro sche Europas (Anura — Froschlurche) — Wittenberg, Lutherstadt: A. Ziemsen
- R Gu Nther
Gu nther R. Die Wasserfro sche Europas (Anura — Froschlurche). — Wittenberg,
Lutherstadt: A. Ziemsen, 1990, — 288 S. — (Die Neue-Brehm-Bu cherei, 600).
Europa ische Wasserfro sche (Anura, Ranidae) und biologisches Artkonzept
- R Gu Nther
Gu nther R. Europa ische Wasserfro sche (Anura, Ranidae) und biologisches Artkonzept //
Mitt. Zool. Mus. Berlin, — 1991. — 67, H. 1. — S. 39–53.
Distribution, population systems and reproductive behavior of green frogs (hybridogenetic Rana esculenta complex) in the Central Chernozem Territory of Russia
- G A Lada
- L J Borkin
- A E Vinogradov
Lada G. A., Borkin L. J., Vinogradov A. E. Distribution, population systems and reproductive behavior of green frogs (hybridogenetic Rana esculenta complex) in the
Central Chernozem Territory of Russia // Russ. J. Herpetol. — 1995. — 2,
N. 1. — P. 46–57.