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Flow cytometry profiles of cellular DNA content of the diploid, triploid, tetraploid, and pentaploid loach Misgurnus anguillicaudatus from Liangzi Lake area, Yangtze River Basin, China.
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A screening of ploidy level in 2146 individuals from 52 populations of the loach Misgurnus anguillicaudatus in China was performed. Ploidy level variation and its geographical distribution in this study was combined with previously reported data from another 28 populations. Two major (2n = 50, 4n = 100) and three minor (3n = 75, 5n = 125, 6n = 150)...
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... level variation of M. anguillicaudatus : A total of 2146 M. anguillicaudatus individuals from 52 populations were examined for ploidy level, and 196 individuals were karyotyped. Five ploidy levels were detected: (1) diploid, the -1 DNA content was 2.49 ± 0.02 pg nucleus , and the chromosome number was 50, consisting of eight metacentrics (m), six submetacentrics (sm), and 36 acrocentrics (a), i.e. karyotype 2n = 50 (8m+6sm+36a); (2) -1 triploid, 3.75 ± 0.04 pg nucleus and 3n = 75 -1 (12m+9sm+54a); (3) tetraploid, 4.96±0.05 pg nucleus and 4n = 100 (16m+12sm+72a); (4) pentaploid, 6.12 ± 0.07 pg -1 nucleus and 5n = 125 (20m+15sm+90a); (5) hexaploid, -1 7.43 ± 0.09 pg nucleus and 6n = 150 (24m+18sm+108a). The representative metaphase cells, and the corresponding karyotype of each ploidy level, are shown in Figure 1. As expected, the major and minor axes of the erythrocytes and their nuclei in different ploidy M. anguillicaudatus increased along with the increasing ploidy level. The cytological parameters of each ploidy level M. anguillicaudatus were summarized in Table 2. Note: The DNA content was calculated using chicken -1 erythrocytes DNA content (2.50 pg nucleus ) as standard. The polyploid M. anguillicaudatus shares the external appearance, i.e. shape and colour, with its sympatric diploid counterparts. The five fin formula was: dorsal fin 2,6; pectoral fin 1,9; pelvic fin 1,5; anal fin 1,6; caudal fin 2,12, no difference among the ploidy levels could be detected. Geographical distribution of different ploidy levels : As shown in Figure 2, diploid M. anguillicaudatus was the dominant ploidy level found in the present study, comprising 65.9% of all indivuduals. Of the 80 populations (52 populations currently sampled and 28 previously reported), 68 included diploids or were exclusively diploids. The second most abundant were tetraploids, accounting for 33.4% of the total. In contrast to the widely distributed diploids, the tetraploids were primarily found in the central Yangtze River basin, especially near the mainstream, including locations 24, 26, 29, 32, 33, and 36. Along the Hanshui tributary in the Yangtze River basin, diploids and tetraploids were observed to coexist in some populations (locations 20, 21, and 22), but interestingly, no triploids were detected. In other populations (locations 8, 9, and 27), a small number of triploids was discovered along with diploids and tetraploids. At each of the locations 45, 51, and 77, only a single triploid co-occurred with diploid individuals. In Shenlongjia area of the Yangtze River basin, ploidy levels varied depending on altitude. At 2500 m (Dajiuhu Lake, location 16), all individuals screened were found to be diploid, while samples from 1200 m (Songbai, location 15) and 600 m (Fangxian, location 14) were only tetraploids. No sympatric population of different ploidy levels were detected in these localities. In Liangzi Lake area, Yangtze River basin (location 30), a single pentaploid individual was found in August, 2011. To verify this phenomenon, 288 additional individuals were collected in two further samplings. Flow cytometric analysis revealed that the tetraploid M. anguillicaudatus was the dominant in the area. Of the 288 individuals, 249 (86.46%) were tetraploid, 32 (11.11%) diploid, four (1.39%) triploid, and three individuals (1.04%) were identified as pentaploid, demonstrating the sympatric occurrence of diploid, triploid, tetraploid, and pentaploid loach. Typical distribution of DNA content in red blood cells (RBC) of polyploid loach from the populations is shown in Figure 3. In the Diaochahu Lake area (location 25), Yangtze River basin, two male hexaploids with 150 chromosomes were detected during May, 2008. No additional hexaploid individual was found, despite repeated screening. No clearly defined geographical ranges or boundaries of the distribution of ploidy levels were found both for diploids and tetraploids. Diploidy is the dominant ploidy level of M. anguillicaudatus in the majority of the Chinese populations assayed in the present and previous studies, as is the case in Japan (Arai, 2003). The tetraploid M. anguillicaudatus is most likely endemic to China, since no tetraploid individual has been identified in wild populations in other countries of eastern Asia (Zhang and Arai, 1999). For a long time, the evolutionary origin of the tetraploid M. anguillicaudatus distributed in the Yangtze River basin, China remained unknown. The recent molecular phylogenetic study of Cobitidae species using nuclear (Slechtova et al ., 2008; Saitoh et al ., 2010) as well as mitochondrial genome sequences (Morishima et al ., 2008; Slechtova et al ., 2008; Koizumi et al ., 2009; Saitoh et al ., 2010; Kitagawa et al ., 2011) indicate that an hybridization event occurred between an ascestral species of Cobitis and ascestral species of Misgurnus early in the evolutionary history of Misgurnus . The interspecific hybridization tends to trigger the development of clonality and gynogenesis, and subsequently, polyploidisation, as well recognized in the spined loaches (Choleva et al ., 2012; Janko et al ., 2012). Therefore, the natural tetraploid M. anguillicaudatus can be regarded as a consequence of this ancient hybridization event. Seven of the 80 studied populations exhibited coexistence of diploids and tetraploids, but a small number of triploids were detected in only three of seven populations, even after repeated sampling. As reciprocal hybridization between natural diploid and tetraploid M. anguillicaudatus can easily produce a large number of triploid progeny (Arai, 2003; Zhou et al ., 2010), the sympatric diploids and tetraploids probably subjected to strong selection pressure to mate with their co-mates, resulted in reproductive isolation of the two- level ploidies. Further research on reproductive isolation between diploid and tetraploid M. anguillicaudatus has not been accomplished yet, but in the striated spined loach (the striata type of the Cobitis taenia complex), researchers found that spawning site segregation is an important factor in reproductive isolation of two sympatric populations- the small and mid-sized forms (Saitoh, 1990). In anuran species, its was reported that females prefer larger males (Sullivan et al. , 1995), or males of a particular size (Robertson, 1990), and researchers have domenstrated the positive relationship between the size of males and females during amplexus in the sunset frog Spicospina flammocaerulea (Smith et al ., 2003) . Researchers concerning spawning behaviour of the loach species argued that, the significantly smaller sized males than females is common characteristic in most genera of Cobitidae, which is a required condition to from a complete ring around the female to activate spawning (Bohlen, 2008). During the studies, we observed that the tetraploid M. anguillicaudatus exhibit obviously larger body size than sympatric diploids, male and female, respectively. Thus, the female-male size ratio may be a factor affecting the reproductive success in this species, either through male- male competition or female mate choice. It is often assumed that polyploids spread because they can better tolerate and invade a wider range of environments than their diploid counterparts, owing to increased genetic buffering provided by additional genome copies (Otto and Whitton, 2000). Greater ecological amplitude has been demonstrated in some polyploid plants compared to their diploid progenitors. Polyploid plants are reported to inhabit regions of higher altitude and tolerate extreme conditions, whereas the lowlands are differentially inhabited by diploid populations. However, this trend may not be the rule in fishes, at least in M. anguillicaudatus. In our results, the diploid M. anguillicaudatus was the dominant ploidy level in most of the sampled localities, showing a broader range than their tetraploid derivatives. Loach from a higher altitude (location 16, Dajiuhu Lake, Shenlongjia area, 2500 m a.s.l.) were exclusively diploid, whereas those from lower altitude (location 15, Songbai, Shenlongjia, 1200 m a.s.l. and location 14, Fangxian, ASL 600 m a.s.l.) were tetraploid. In addition, the tetraploid M. anguillicaudatus has a conspicuously bigger adult body size than the diploid form (Zhou et al ., 2010), and, as a consequence, the fecundity of tetraploids is higher than that of diploids. However, the occurrence of tetraploids in natural populations of M. anguillicaudatus is relatively low, possibly indicating that the increased cell surface of ...
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Citations
... The sex identification of weather loach was based on the morphological sexual dimorphism: the males have a small bony plate on each pectoral fin that the females don't have [31]. Because there are natural diploid and tetraploid populations in Misgurnus anguillicaudatus [32,33], we employed a flow cytometry (CyFlow Space, Sysmex Partec, Germany) to detect the DNA content of erythrocytes to determine the ploidy status of each sample. The peripheral blood of each loach was collected from the tail vein using a syringe. ...
The release and sensation of sex pheromone play a role in the reproductive success of vertebrates including fish. Previous studies have shown that the weather loach Misgurnus anguillicaudatus perceives sex pheromones by olfaction to stimulate courtship behavior. It was speculated that weather loaches use smell to recognize intraspecific mates. However, the identification of loach pheromone receptor has not been reported. By comparative transcriptomic approach, we found that the olfactory receptor gene or114-1 was male-biasedly expressed in the olfactory epithelium of M. anguillicaudatus, M. bipartitus and the closely related species Paramisgurnus dabryanus. This sex-biased expression pattern implicated that or114-1 presumably encoded a sex pheromone receptor in loaches. M. bipartitus and P. dabryanus, like zebrafish, possess one or114-1 only. However, in M. anguillicaudatus, or114-1 has two members: Ma_or114-1a and Ma_or114-1b. Ma_or114-1a, not Ma_or114-1b, showed sex-differential expression in olfactory epithelium. Ma_or114-1b has base insertions that delayed the stop codon, causing the protein sequence length to be extended by 8 amino acids. Ma_or114-1a was subject to positive selection resulting in adaptive amino acid substitutions, which indicated that its ligand binding specificity has probably changed. This adaptive evolution might be driven by the combined effects of sexual selection and reinforcement of premating isolation between the sympatric loach species.
... Since then, researchers found that, along with diploids (2n ¼ 50), which are the most common, some wild loach populations in Japan also contain relatively high proportions of triploid loaches [12,13]. In China, tetraploid M. anguillicaudatus were frequently recorded in addition to the most widespread diploids [14,15], and small proportions of triploids have been detected at several locations [16]. Some studies have also reported the existence of specimens with rare ploidy levels, including pentaploids (5N ¼ 125) [17] and hexaploids (6N ¼ 150) [16]. ...
... In China, tetraploid M. anguillicaudatus were frequently recorded in addition to the most widespread diploids [14,15], and small proportions of triploids have been detected at several locations [16]. Some studies have also reported the existence of specimens with rare ploidy levels, including pentaploids (5N ¼ 125) [17] and hexaploids (6N ¼ 150) [16]. Although the polyploidy phenomenon has received ample scientific attention, previous studies of ploidy level variation and geographical distribution of polyploid loaches in China were limited to specific localities or regions. ...
... Flow cytometry (FCM) is an accurate and convenient method to detect variation in the ploidy level in large samples [23]. We collected blood from the tail vein mainly following the protocol described by Yu et al. [16]. Blood cells were suspended in 1 ml staining buffer (Cystain DNA 1 step staining solution) for 3 min. ...
The origin and evolution of polyploid organisms have been extensively studied in plants, but this topic remains only partially understood in vertebrates, where polyploidy is relatively rare. In this study, we used Misgurnus anguillicaudatus, a fish that comprises five ploidy levels in nature, as a model animal to improve our understanding of biogeographic history and evolution of polyploid vertebrates. After collecting samples from different geographical populations in China, their ploidy levels were determined using flow cytometry. Two mitochondrial markers ( cytochrome b and control region) were then used for phylogeographic analyses to unravel the possible origins of diploids and tetraploids in China. The results showed that diploids have wider geographical distribution than tetraploids and triploids. There was no clear allopatric geographical range or boundary to divide diploid and polyploid populations. Rather, the analysis of mitochondrial DNA sequences indicated that tetraploids were autopolyploids, with lower genetic diversity than diploids. This suggests that tetraploids originated from sympatric diploids via multiple independent polyploidization events. Genetic structure patterns were similar between diploids and tetraploids, whereas complex genetic differentiation was found among different regions. The potential origin of M. anguillicaudatus was deduced to be in the Pearl River basin, which exhibited the highest nucleotide diversity and genetic differentiation. These findings provide insights into the evolution of polyploidy in vertebrates.
... In the following, DNA content of the blood samples were stained with propidium iodide and fluorescent peaks were specified by using yellow fluorescent filter (FL2). Finally, total cellular DNA amounts of diploid and triploid trouts were compared each other by using fluorescent peaks (Yu, Abbas, Wang, & Zhou, 2014). Samples were illuminated with laser argon ion at 488nm and detection was done in 650nm via fluorescence detector (FL2). ...
Triploid fish production has become important in the aquaculture sector, especially in the culturing and breeding of the big sized Salmonid species. Black Sea trout (Salmo labrax) is one of the promising Salmonid species for these purposes considering increased demand for this species in the aquaculture sector. In this research, triploid Black Sea trout were treated with heat shocks during reproduction and triploidy of obtained trouts were identified with different techniques. For this reason, heat shocks were applied at 26.5°C, 28°C and 36°C temperatures for 10 minutes during 30th minute of fertilization and triploidy was determined with fragment analysis, flow cytometry and classic hematological methods. Results indicate that all three temperatures were suitable for the successful reproduction of Black Sea trout. However, 26.5°C gives better results considering both the triploidy success and survival rates. Besides, all three determination techniques especially erythrocyte size measurements and flow cytometry can be used in evaluating of triploidy in Black Sea trout with precise results.
... Arai [3] reported that besides the most common bisexual diploid individuals (2n = 50), a relatively high frequency of asexual diploid clones and natural triploids (3n = 75) were also observed in certain localities in Japan. Among Chinese M. anguillicaudatus populations, in addition to the most common sexual diploids, large numbers of tetraploids (4n = 100) have been recorded along the Yangtze River basin [9][10][11]. Experimental crosses, including induced gynogenesis [12][13], androgenesis [14], hexaploids [15], and observations of the meiotic behavior of chromosomes [16] suggest an autotetraploid origin of the natural tetraploids. ...
... To validate the selected ploidy diagnostic EST-SSR markers, 96 ploidy-unknown individuals were randomly collected from the Liangzi Lake (Fig 1), a locale with mixed ploidy population (primarily diploids and tetraploids) [11,30]. For each individual, a small piece of caudal fin was cut and stored in 75% ethanol; genomic DNA was extracted using ammonium acetate method [31]. ...
The co-existence of several ploidy types in natural populations makes the cyprinid loach Misgurnus anguillicaudatus an exciting model system to study the genetic and phenotypic consequences of ploidy variations. A first step in such effort is to identify the specific ploidy of an individual. Currently popular methods of karyotyping via cytological preparation or flow cytometry require a large amount of tissue (such as blood) samples, which can be damaging or fatal to the fishes. Here, we developed novel microsatellite markers (SSR markers) from M. anguillicaudatus and show that they can effectively discriminate ploidy using samples collected in a minimally invasive way. Specifically, we generated whole genome transcriptomes from multiple M. anguillicaudatus using the Illumina paired-end sequencing. Approximately 150 million raw reads were assembled into 76,544 non-redundant unigenes. A total of 8,194 potential SSR markers were identified. We selected 98 pairs with more than five tandem repeats for further assays. Out of 45 putative EST-SSR markers that successfully amplified and harbored polymorphism in diploids, 11 markers displayed high variability in tetraploids. We further demonstrate that a set of five EST-SSR markers selected from these are sufficient to distinguish ploidy levels, by first validating them on 69 reference specimens with known ploidy levels and then subsequently using fresh-collected 96 ploidy-unknown specimens. The results from EST-SSR markers are highly concordant with those from independent flow cytometry analysis. The novel EST-SSR markers developed here should facilitate genetic studies of polyploidy in the emerging model system M. anguillicaudatus.
... In a recent study, Yu et al. (2014) describe the variation of ploidy forms of Misgurnus anguillicaudatus (Cobitidae) depending of altitude gradient. Where, the occurrence of ploidy forms can assume the differences at the microhabitat compositions also. ...
Loaches (genus Cobitis) in Slovakian tributaries (Danube River Basin) are represented by diploid-polyploid hybrid
complexes of C. elongatoides and C. tanaitica. Uniquely, their coexistence is made possible by the presence of
polyploid (mainly triploid) females that are sexually dependant on diploid male sperm (donors) for gynogenesis.
Information on the spatial distribution of Cobitis with of differing ploidy remains relatively scarce. The main aim
of this study, therefore, was to identify in ploidy in the species preferred microhabitat. Overall, 345 Cobitis were
recorded in Rivers Okna and Ondava (Danube Basin) between 2011 and 2015, with 316 diploid and triploid
individuals detected by flow cytometry examined were studied for the microhabitat preferences with the using
the point sample method. The sex ratio differed significantly between localities, while diploid-polyploid ratio
not. Moreover, each of ploidy-sex forms (i.e. diploid male, diploid female, triploid female) showed a preference
for a specific substrate composition, velocity, depth and distance from the bank at both localities. Mixed effect
linear models identified clear differences in fine substrate between seasons for individuals from the River Okna.
Similarly, non-metric multidimensional scaling detected differences in environmental variables preference for
both diploid and triploid forms. These finding indicate specific spatial and temporal microhabitat preference for
diploid (sexual donors) and triploid (asexuals) C. elongatoides ×C. tanaitica when coexisting as mixed a population.
... Weatherfishes, from the genera Misgurnus and Paramisgurnus, are a group of small benthic loaches living in rivers, lakes, ponds and paddy fields that are distributed across East Asia and Central Europe [12]. The genus Misgurnus is composed of several nominal species, among which Misgurnus anguillicaudatus occurs primarily in southern East Asia and is regarded as a species complex because it consists of both diploid and tetraploid populations, which are morphologically indistinguishable from each other [13]. Misgurnus bipartitus is distributed in northern East Asia and exhibits a largely parapatric distribution pattern with M. anguillicaudatus currently. ...
... The sexes of individual loaches were determined based on sexual dimorphism, as mature males exhibit a bony plate in each pectoral fin [15]. Because there are both diploid and polyploid populations of M. anguillicaudatus [13], flow cytometry analysis using erythrocytes was performed to determine the ploidy status of the samples according to Yu et al. [13]. The loaches were preserved in 95% ethanol after being anaesthetized in a solution of 200 mg/L tricaine methanesulfonate (MS-222; Sigma-Aldrich, Saint Louis, MO, USA). ...
... The sexes of individual loaches were determined based on sexual dimorphism, as mature males exhibit a bony plate in each pectoral fin [15]. Because there are both diploid and polyploid populations of M. anguillicaudatus [13], flow cytometry analysis using erythrocytes was performed to determine the ploidy status of the samples according to Yu et al. [13]. The loaches were preserved in 95% ethanol after being anaesthetized in a solution of 200 mg/L tricaine methanesulfonate (MS-222; Sigma-Aldrich, Saint Louis, MO, USA). ...
In contrast to other olfactory receptor families that exhibit frequent lineage-specific expansions, the vomeronasal type 1 receptor (V1R) family exhibits a canonical six-member repertoire in teleosts. V1r1 and V1r2 are present in no more than one copy in all examined teleosts, including salmons, which are ancient polyploids, implying strict evolutionary constraints. However, recent polyploids have not been examined. Here, we identified a young allotetraploid lineage of weatherfishes and investigated their V1r1-V1r2 cluster. We found a novel pattern that the parental V1r1-V1r2 clusters had recombined in the tetraploid genome and that the recombinant was nearly fixed in the tetraploid population. Subsequent analyses suggested strong selective pressure, for both a new combination of paralogs and homogeneity among gene duplicates, acting on the V1r1-V1r2 pair.
... However, asexual diploid clones and natural triploids (3n = 75) are also observed in certain localities ; Morishima e t a l . 2 0 0 2 ; Arai 2 0 0 3 ) . A m o n g C h i n e s e M. anguillicaudatus populations, in addition to the most common sexual diploids, large numbers of tetraploids (4n = 100) have been recorded in the wild along the Yangtze River basin (Li et al. 1983;Yu et al. 1989;Yin et al. 2005;Li et al. 2008;Yu et al. 2014). Experimental crosses, including induced gynogenesis (Arai et al. 1991(Arai et al. , 1993, androgenesis (Arai et al. 1995), and hexaploids , and observations of the meiotic behavior of chromosomes (Li et al. 2011) suggest an autotetraploid origin of the natural tetraploids. ...
... Experimental crosses, including induced gynogenesis (Arai et al. 1991(Arai et al. , 1993, androgenesis (Arai et al. 1995), and hexaploids , and observations of the meiotic behavior of chromosomes (Li et al. 2011) suggest an autotetraploid origin of the natural tetraploids. These tetraploid populations are sometimes found in sympatry with diploid populations, yet the lack of triploid individuals suggests that diploid and tetraploid populations are reproductively isolated from each other Yu et al. 2014;Zhong et al. 2015). Thus, Chinese M. anguillicaudatus in a diploid-tetraploid complex (Li et al. 2011) is an extremely promising animal model for studying genetic and phenotypic consequences of ploidy variations in fish. ...
... However, despite the long-recognized extensive karyotype polymorphisms in natural populations of M. anguillicaudatus, the biological and ecological differences between these distinct ploidy forms remains poorly understood (Li et al. 1983;Arai 2003;Yin et al. 2005;Zhou et al. 2008;Yang et al. 2009;Yu et al. 2014), primarily due to the difficulty in distinguishing different ploidy forms using morphological characteristics Zhou et al. 2008). However, as has been described in the spined loach Cobitis taenia (Juchno and Boroń 2010) and Iberian minnow Squalius alburnoides (Ribeiro et al. 2003), biologically and ecologically relevant differences may occur in the coexisting diploid-polyploid complex (Schenck and Vrijenhoek 1989). ...
Diploids and tetraploids of the cyprinid loach Misgurnus anguillicaudatus coexist in many natural habitats in Asia. However, little is known about the biological and ecological differences between these two ploidy forms. We examined age, body size and growth rates of fish in a mixed ploidy population of M. anguillicaudatus in the Yangtze River basin in China. The sex ratios of both diploid and tetraploid M. anguillicaudatus were highly skewed toward females, who tended to be larger than males. The age distributions of the collected specimens clearly indicated that tetraploids lived longer than diploids. For example, we found a substantial number of tetraploids that were 5+ years old, while the oldest diploids were 4+ years old. Tetraploids were also longer and heavier than diploids for both sexes. Using the empirical body size and age data, we inferred the growth patterns of these fish with the von Bertalanffy growth function. The estimated asymptotic body lengths (L∞) indicated that tetraploids could indeed achieve larger body sizes than diploids. This difference was partially due to the increased growth rate, as demonstrated by lower growth coefficient (K) and higher growth performance index (φ’). In sum, we show that tetraploid M. anguillicaudatus exhibited significantly increased longevity and superior growth performance compared to diploids. These differences may contribute to the ecological competitiveness of tetraploid M. anguillicaudatus, thus enabling them to coexist with diploids in certain ecological settings.
... The loach Misgurnus anguillicaudatus , widespread in Eurasia, is regarded as an excellent animal model to explain the biological origin and evolutionary significance of polyploidization and unisexual reproduction because of its complex ploidy composition [Li et al., 2008;Yu et al., 2014] and abnormal ploidy of the gametes . Five different ploidy levels are found in loaches in China, including diploidy, triploidy, tetraploi- ...
The gynogenesis phenomenon in nature mainly appears in the reproduction of fish and invertebrates. So far, gynogenesis has been successfully induced in many fish species with the aid of some physical or chemical methods for chromosome doubling. However, few fish can produce gynogenetic progenies, genetically identical or similar to the somatic cells of the mothers, without a treatment for the doubling of chromosomes, which may be related to apomixis, premeiotic endoreduplication, or premeiotic endomitosis. At present, no studies are available about fish with normal ovarian structures producing gynogenetic progenies that could spontaneously double their chromosomes. According to the analyses of flow cytometry, chromosome number, and microsatellites, we found that, with the use of UV-irradiated sperm of blunt snout bream Megalobrama amblycephala, tetraploid loach Misgurnus anguillicaudatus produced tetraploid gynogenetic progenies without any treatments for the doubling of chromosomes. To determine the genetic relationships of gynogenetic progenies and their maternal parent, microsatellite genotyping was conducted. The results indicated that the reason for spontaneous chromosome duplication in gynogenetic progenies may be cytokinesis or inhibition of the extrusion of the second polar body. This is the first report on fish with normal ovarian structures that can produce gynogenetic progenies which spontaneously double their chromosomes and which are genetically identical or similar to the somatic cells of the mothers.
