Speciation is a continuous process, often progressing with decreasing gene flow between diverging populations. According to the concept of the speciation continuum (Shaw and Mullen, 2014; Stankowski and Ravinet, 2021), hybridization between relatively closely related lineages typically results in fertile and recombining progeny and may even lead to an evolutionary meltdown or homoploid hybrid speciation (Comeault and Matute, 2018). Increasing genetic divergence between hybridizing taxa may further promote the emergence of transgressive phenotypes (Stelkens and Seehausen, 2009) or hybrid vigour but typically lowers the mean fitness of hybrids, which consequently impacts the establishment of postzygotic reproductive isolating barriers (Comeault and Matute, 2018). In species with well-differentiated sex chromosomes, incompatibilities particularly affect the heterogametic sex (Haldane’s rule) (Haldane, 1922; Welch, 2004; Stöck et al., 2021). Ultimately, speciation is completed when the accumulation of incompatible alleles in differentiating populations induces hybrid sterility or even inviability.

However, hybridization is also known to give rise to fertile, yet asexually reproducing hybrids in various animal and plant taxa. Asexual hybrids exhibit a broad spectrum of cytological mechanisms for the production of unreduced, often clonal, gametes, which range from entirely ameiotic processes (apomixis) to those involving more or less distorted meiosis (automixis; Neaves and Baumann, 2011; Dedukh et al., 2022b). A relatively common gametogenic alteration leading to asexuality is premeiotic genome endoreplication (Figure 1), found in a variety of hybrid fishes, amphibians, and reptiles (Macgregor and Uzzell, 1964; Itono et al., 2006; Lutes et al., 2010; Dedukh et al., 2020; Dedukh et al., 2022a). By auto-duplication, from each chromosome usually an identical copy is produced to pair with during the meiotic prophase. Premeiotic genome endoreplication thus not only ensures clonal reproduction, but also allows hybrids to overcome problems in chromosome pairing that would otherwise lead to their sterility (Dedukh et al., 2020; Janko et al., 2018). Hybridization and asexuality thus represent important evolutionary phenomena (Neaves and Baumann, 2011).

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To explain the apparent link between asexuality and hybridization, the ‘balance hypothesis’ has been proposed (Moritz et al., 1989), which assumes that incompatibilities, accumulated among parental genomes, may disturb gametogenesis in hybrids leading to the formation of unreduced gametes. Hybrid asexuality may thus emerge in a ‘favourable evolutionary window’ of genetic divergence between hybridizing species, which should be large enough to trigger particular gametogenic aberrations, but not too large to compromise the hybrid’s fertility or even viability. The recently proposed concept of the ‘extended speciation continuum’ (Stöck et al., 2021) explicitly links the emergence of asexual reproduction to the speciation continuum. While forming species ultimately reach complete intrinsic reproductive isolation under increased divergence, fertile hybrids may be produced at earlier stages that exhibit aberrant gametogenesis, leading towards clonal reproduction. This not only facilitates the formation of allodiploid and allopolyploid asexual hybrid lineages, but asexuality per se also effectively restricts introgression between parental species due to non-recombinant production of gametes. Hybrid asexuality may thus be considered a particular type of Bateson-Dobzhansky-Muller (BDM)-incompatibilities, representing a form of intrinsic reproductive isolation during the speciation process (Janko et al., 2018).

While the evolutionary link between hybridization and asexuality has been empirically documented, it remains unclear how widespread such a link is and how commonly might asexual gametogenesis occur in hybrids. On the one hand, naturally occurring asexual hybrids exist in many major animal and plant lineages, but appear rare, suggesting that the genomic pre-conditions required for asexual reproduction may be rarely met during hybridization (Stöck et al., 2010). On the other hand, most of the knowledge about the evolution and biology of asexual hybrids comes from studies of naturally occurring lineages, while laboratory crossing experiments have been rarely performed to directly address the rate of clonal gametogenesis in hybrids. The questions how easily asexual reproduction is induced and why it is so often linked with a hybrid constitution thus remains unclear.

To estimate the incidence of clonal gametogenesis in a radiation of freshwater fish, we performed extensive crossing experiments of sexual species and investigated the gametogenic pathways in their hybrids, using European spined loaches of the family Cobitidae as a model. Cobitidae presents a speciose group of freshwater fish of Southeast Asian origin that spread over most of the Palearctic region since late Eocene (Bohlen et al., 2019). They colonized Europe in four distinct lineages (Perdices et al., 2016), which diverged from each other around 17–20 Mya (Perdices et al., 2016; Majtánová et al., 2016). The so-called Adriatic and Bicanestrinia lineages colonized Southern Europe and Near East regions, while Central and Eastern Europe have been colonized by the Cobitis sensu stricto lineage (Figure 1a–b). This lineage is composed of two sub-groups, the so-called C. taenia clade, involving several closely related species diverged during the last 1 Mya, and C. elongatoides, which diverged ~9 Mya from the C. taenia clade (Janko et al., 2018). Such independent colonization events and subsequent range shifts gave rise to natural hybrid zones particularly across Central and Eastern Europe (Janko et al., 2012). Diploid and polyploid hybrids have been reported within the family, including gynogenetic ‘asexual’ lineages. These lineages reproduce via gynogenesis, that is clonal eggs require sperm from sexual males to activate further development into genetically identical progeny. After fertilization, male pronucleus is usually eliminated from the eggs, without genetic contribution to the progeny (Yamashita et al., 1990; Fyon et al., 2023; Figure 1a–c). Such forms usually discard the sperms ’genome after fertilization and are currently found in hybrids of the Asian Misgurnus anguillicaudatus complex (Morishima et al., 2008), the Cobitis hankugensis-longicorpa hybrids in Korea (Kim and Lee, 1995), and in hybrids of the European Cobitis sensu stricto lineage (Figure 1b, Choleva et al., 2012). In these natural systems, only hybrid females are known to produce unreduced gametes, employing premeiotic genome endoreplication, while hybrid males are usually sterile due to aberrant pairing of chromosomes in meiosis (Dedukh et al., 2020; Dedukh et al., 2021).

In the present paper, we report meiotic and premeiotic gametogenic stages of experimental hybrids of eight loach species, representing three main European lineages. These species have been crossed in various combinations from closely related taxa to phylogenetically distant ones, which allowed us to test, how often unreduced hybrid gametes arise, whether their emergence is linked to genetic and karyotypic divergence between parental species, and how asexuality is related to hybrid sterility.

Using freshwater fishes, loaches (Cobitidae), as a model, the present study reveals a wide range of reproductive outcomes in F1 hybrids in relation to genetic and karyotype divergences between the parental species (Figure 6). On one extreme, hybrid inviability has been reported in crosses between distant species (Suzuki, 1957). On the other extreme, the production of haploid gametes was found in crosses of closely related species, such as between C. lutheri and C. tetralineata (Kwan et al., 2019), and between C. pontica and C. taenia Janko et al., 2018 or C. tanaitica species, whose divergence has been dated to ~1 Mya Janko et al., 2018, but also in OB female hybrids in a relatively distant species pair (Figure 2, Figure 6, Figure 4—figure supplement 1d, Figure 4—figure supplement 2d). However, the most common types of reproductive outputs were hybrid sterility and production of unreduced gametes.

In case of hybrids between relatively far-distant species pairs, like the intergeneric Cobitis-Misgurnus cross, or between Adriatic and Cobitis sensu stricto lineages (i.e. EB and TB hybrids), sterility occurred in hybrids of both sexes (Figure 6). However, the most common outcome was asymmetric, with sterility affecting hybrid males, while F1 females produced unreduced oocytes. This pattern occurred in the majority of crosses, including species pairs, like SE, SP or EO, with divergences reaching ~17 or even >20 Mya back (Majtánová et al., 2016; Figure 2, Figure 6) and it has also been reported from several natural hybrid complexes (Itono et al., 2006; Dedukh et al., 2020; Dedukh et al., 2021). An intermediate situation was observed in TP-hybrids between a closely related species that diverged ~1 Mya (Janko et al., 2018), where males produced reduced gametes and females produced both, reduced and unreduced ones.

It is generally assumed that the emergence of asexuality is a rare phenomenon that may require complex changes in gametogenic pathways and reproductive modes (Stöck et al., 2010). This opinion has been corroborated by the ‘twiggy’ distribution of ‘asexual’ organisms on the tree of life (Schwander and Crespi, 2009) and by many failures to re-generate naturally occurring asexual hybrids by experimental crosses of their parental species (e.g. in apomictic Poecilia fish and parthenogenetic Darevskia lizards Stöck et al., 2010; Murphy et al., 2000). However, we observed the production of unreduced gametes in 7 out of 11 crossed species pairs of loaches and in 10 out of 18 species pairs when including literature reports and natural hybrids (Figure 2, Figure 6). Such a widespread emergence of asexual gametogenesis therefore appears not to depend on the presence of a genome from any particular parental species, but to arise relatively commonly among independent species pairs across the entire group of spined loaches. Asexual gametogenesis has also been observed in experimental F1 progeny of several other vertebrate species (Iwai et al., 2011). This suggests that the formation of unreduced gametes, that is the necessary prerequisite for asexual reproduction, may be a much more common outcome of interspecific hybridization than it would appear from the rarity of asexual hybrid taxa that are successfully established in nature.

Some studies also suggested that the emergence of asexuality requires the evolution of specific genes within hybrid lineages after their origin (Alberici da Barbiano et al., 2013). However, our finding that asexual gametogenesis originates relatively commonly already in the F1 generation somewhat refines this hypothesis and suggests that it is a direct result of genome merging by interspecific hybridization. Importantly, all F1-females capable of clonal gametogenesis employed an identical cytogenetic mechanism, i.e. premeiotic genome endoreplication, as also observed in many natural asexual vertebrates (Betto-Colliard et al., 2018; Itono et al., 2006; Dedukh et al., 2020; Dedukh et al., 2022a; Dedukh et al., 2021; Iwai et al., 2011; Bi and Bogart, 2010; Stöck et al., 2012) suggesting that gametogenic perturbations induced by hybridization are often canalised into a similar developmental pathway. The reasons for such common patterns are not clear. The regulation of cell cycle is particularly sensitive to stress and perturbations (Rotelli et al., 2019) and interspecific hybridization may act as such stimulus (Moritz et al., 1989). While asexual reproduction may employ various pathways (Neaves and Baumann, 2011), it is possible that aberrations of cell cycle leading to endoreplication are more common since they require less accumulated incompatibilities than other routes to the production of unreduced gametes. Alternatively, the occurrence of endoreplication may reflect some predispositions, like the spontaneous production of unreduced gametes in some sexual parental lineages, which would then ensure clonal reproduction in their hybrids. However, our data argue against this alternative, since we analysed hundreds of gonocytes of sexual females without a single incidence of genome endoreplication (Dedukh et al., 2020; Dedukh et al., 2021). Moreover, during years of crossing experiments and population sampling, we genotyped hundreds of C. elongatoides and C. taenia and their progenies and never found an autotriploid specimen (Janko et al., 2012; Tichopád et al., 2022), which would be expected if fertilisation of unreduced gametes existed in these species (Flajšhans et al., 2007).

Our in-depth analysis of hybrid gametogenesis in Cobitis loaches further provided compelling evidence for a tight link between hybrid incompatibility, asexuality and sterility. Namely, the majority of meiocytes produced by both the male and female hybrids failed to form a full set of bivalents between orthologous chromosomes and were arrested at meiotic checkpoints (Figure 3). However, unlike their sterile brothers, hybrid F1 females also usually contained a minor proportion of oogonia that underwent premeiotic genome endoreplication. In most our F1 hybrid females, only these rare oogonia were able to complete meiosis and form diploid gametes. Interestingly, similar observations were reported from several natural and experimental hybrid vertebrates, like ET and EN hybrid loaches, geckos and whiptail lizards (Aspidoscelis) Medaka ricefish (Oryzias) (Dedukh et al., 2022a; Dedukh et al., 2021; Iwai et al., 2011; Newton et al., 2016). This suggests that even successfully established hybrid asexuals usually contain only a minor proportion of oogonia, which actually undergo clonal gametogenetic pathway.

Such congruent patterns across phylogenetically distant taxa thus conform to the concept of an ‘extended speciation continuum’. Similar to the classical concept of the ‘speciation continuum’, it assumes that speciation generally proceeds from early stages characterized by the production of sexual hybrid progeny to irreversibly diverged species, whose hybrids are either sterile or even inviable. At intermediate stages, however, hybrids between diverging evolutionary lineages may not only have a certain incidence of sterile gonocytes, but also tend to produce unreduced gametes (Figure 6). Genome endoreplication thus appears as an effective way to overcome sterility in hybrid females, even at high levels of divergence. Asexuality may thus often represent the only reproductive pathway of hybrids between a given pair of species and, together with hybrid sterility, it may simultaneously contribute to reproductive isolation of parental species due to clonal genome propagation.

We observed that the fertility of female hybrids remains conserved due to sex-specific emergence of clonality, while males of the same cross are usually sterile. This may potentially indicate some analogy to other classical sex-related asymmetries in hybrids, like incompatibilities between sex chromosomes (Haldane’s rule) or other uniparentally inherited factors (Darwin’s corollary Brandvain et al., 2014). However, the sex determination systems are not yet known in most of the investigated species (Stöck et al., 2021) and in any case, the reasons for such an asymmetry are likely more complex. For instance, meiocytes in hybrid males contained significantly lower numbers of properly-formed synaptonemal complexes than non-duplicated meiocytes in females (Figure 5) and were more severely affected by decreasing similarity of parental karyotypes (see Results, 2.3.5.). This indicates some more fundamental differences in pairing mechanisms and affinity among orthologous chromosomes fundamentally between spermatogenesis and oogenesis, e.g. (Blokhina et al., 2019). In fact, we recently found that spermatogonial cells taken from a sterile ET hybrid male may resume the ability of endoreplication when transplanted into female gonads (Tichopád et al., 2022). This suggests that initiation of premeiotic endoreplication may rely on female-specific gonadal environment rather than on genetic sex determination.

The genetic divergence among parents may affect early gametogenic stages in hybrids through various mechanisms causing for example depletion of primordial germ cells (Yoshikawa et al., 2018), improper pairing of diverged chromosomes (Ferree and Prasad, 2012), asynapsis between sex chromosomes (Bhattacharyya et al., 2013), or deleterious epistatic interactions between orthologous genes and their binding motifs on chromosomes (Balcova et al., 2016). In loaches, we documented at least two such mechanisms underlying hybrid sterility. TB and PS hybrid males had almost no spermatocytes, suggesting their gonocytes probably failed the transition to meiosis. The other type of sterility conforms to a chromosomal speciation model (Faria and Navarro, 2010; Potter et al., 2017), prevailing in most F1 hybrid males, in which spermatocytes developed but possessed aberrantly paired chromosomes, preventing further progression to spermatids. Analogous patterns were observed in non-duplicated oocytes of most hybrid females, suggesting that problems in bivalent-formation have a detrimental impact on the meiosis in both male and female loach hybrids.

Karyotype evolution among parental species indeed plays a crucial role in hybrids’ reproductive capabilities (Potter et al., 2017). Our data suggest that it has a crucial, yet indirect, impact on asexual reproduction. Specifically, hybrids between species with diverged karyotypes had less bivalents in non-duplicated meiocytes than those combining similar karyotypes. Sometimes, even hybrids between phylogenetically distant, yet karyotypically similar species could produce full sets of bivalents (e.g. OB hybrids; Figure 5). On the other hand, the numbers of endoreplicated oocytes were low in any hybrid. Their proportion was relatively higher in natural clones than in experimental F1 Cobitis, suggesting that such a trait may recover during the evolutionary establishment of a natural asexual lineage (Dedukh et al., 2021) and/or that selection among ‘freshly’ emerged clones would favour those with the highest proportion of endoreplicated oocytes. Nevertheless, even the most widespread clones possessed only ~6% of such oogonia, suggesting that karyotype similarity allows the completion of meiosis and hybrids would mostly reproduce sexually by reduced gametes, even if they had the capacity of producing unreduced gametes, too.

While hybridization is assumed to present an important trigger of asexuality in vertebrates and other organisms (Neaves and Baumann, 2011), the origins of clonal lineages are thought to be rare, and often can be traced back to a single or few hybridization events in a given species pair (Stöck et al., 2010; Choleva et al., 2012). Multiple independent origins of clonal gametogenesis in spined loaches (Janko et al., 2012; Choleva et al., 2012, this study) in part contradicts this view since interspecific hybridization has been found to result in clonal gametogenesis relatively commonly up to a substantial divergence, where fertile or viable hybrids are no longer appearing (Figure 6a). However, we emphasize that successful establishment of hybrid clones under natural conditions is likely restricted by several additional levels of selective pressure and thus filtering (Figure 6b). On the one hand, the ‘balance hypothesis’ (Moritz et al., 1989) and its expansions and fine-tuned versions (Janko et al., 2018; Stöck et al., 2010), suggest that the production of unreduced gametes probably requires some level of genetic divergence among the parental species to alter the hybrid cell cycle towards genome endoreplication. On the other hand, it appears that most meiocytes of asexual hybrids anyway do not pass through endoreplication (Dedukh et al., 2022a; Dedukh et al., 2021; Iwai et al., 2011; Newton et al., 2016). Consequently, if the parental karyotypes remain largely similar, then orthologous chromosomes may successfully pair even in such nonduplicated meiocytes, potentially, allowing them to accomplish normal meiosis and form reduced gametes. This would decrease the proportion of unreduced gametes produced by such hybrids and negatively impact on their likelihood to establish a stable asexual lineage.

We therefore propose, that for a cross to be successful in generating an asexual hybrid, it not only has to produce a sufficient number of unreduced gametes, but it also has to prevent the formation of reduced gametes from non-duplicated meiocytes. One way to achieve this may be if hybridization involves species with sufficiently diverged karyotypes, ensuring improper pairing of orthologous chromosomes in non-duplicated gametes. Increased divergence of parental karyotypes may therefore have a positive impact on the production of stable clonal hybrids and, for instance, the fixation of certain chromosomal rearrangements among diverging populations may be accelerated by certain geographical aspects of speciation, such as parapatry (Faria and Navarro, 2010; Potter et al., 2017). It would thus be attractive to test if the incidence of asexual hybrids correlates with increased rates of karyotype evolution among parental species.

The rarity of naturally occurring clonal organisms probably results from the simultaneous impact of the abovementioned selective processes. However, our data indicate that the production of unreduced gametes, which is the very basic conditio sine qua non for the evolution of asexuality, may be surprisingly ‘easy’ to trigger, especially in hybrids of distantly related lineages. Of course, we may not rule out that the frequent emergence of premeiotic endoreplication in Cobitidae reflects some specific predispositions in their gametogenic machineries in comparison to other taxa, where asexuality appears rarer. Thus, our study demonstrates that conclusions about the evolution of asexuality should not only be drawn from natural asexuals, but should be based also on experimental crosses.

The genomic sequence data generated and analyzed during the current study are available in the NCBI repositories with the bioproject ID PRJNA1025348 and the following accession numbers: C. elongatoides: SAMN37721543, C. taenia: SAMN37721544, C. taurica: SAMN37721545, C. tanaitica: SAMN37721546, C. pontica: SAMN37721547, C. ohridana: SAMN37721548, C. strumicae: SAMN37721551, C. bilineata: SAMN37721552.

1. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721543. Model organism or animal sample from Cobitis elongatoides.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721543
2. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721544. Model organism or animal sample from Cobitis taenia.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721544
3. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721545. Model organism or animal sample from Cobitis taurica.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721545
4. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721546. Model organism or animal sample from Cobitis tanaitica.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721546
5. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721547. Model organism or animal sample from Cobitis pontica.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721547
6. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721548. Model organism or animal sample from Cobitis ohridana.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721548
7. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721551. Model organism or animal sample from Cobitis strumicae.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721551
8. 1. Janko K

   (2023) NCBI BioSample

   ID SAMN37721552. Model organism or animal sample from Cobitis bilineata.

   https://www.ncbi.nlm.nih.gov/biosample/SAMN37721552

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Author details

1. Anatolie Marta

   Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CAS, Libechov, Czech Republic

   Contribution

   Conceptualization, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   anatolmarta@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4457-8838

2. Tomáš Tichopád

   Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CAS, Libechov, Czech Republic

   Contribution

   Software, Formal analysis

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9154-2969

3. Oldřich Bartoš

   Military Health Institute, Military Medical Agency, Prague, Czech Republic

   Contribution

   Data curation, Software, Formal analysis

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5441-5592

4. Jiří Klíma

   Laboratory of Cell Regeneration and Plasticity, Institute of Animal Physiology and Genetics of the CAS, Liběchov, Czech Republic

   Contribution

   Methodology

   Competing interests

   No competing interests declared

5. Mujahid Ali Shah

   Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in Ceske Budejovice, Vodnany, Czech Republic

   Contribution

   Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5727-7164

6. Vendula Šlechtová Bohlen

   Laboratory of Fish genetics, Institute of Animal Physiology and Genetics of the CAS, Liběchov, Czech Republic

   Contribution

   Formal analysis, Methodology

   Competing interests

   No competing interests declared

7. Joerg Bohlen

   Laboratory of Fish genetics, Institute of Animal Physiology and Genetics of the CAS, Liběchov, Czech Republic

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

8. Karel Halačka

   Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CAS, Libechov, Czech Republic

   Contribution

   Methodology

   Competing interests

   No competing interests declared

9. Lukáš Choleva

   Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic

   Contribution

   Methodology

   Competing interests

   No competing interests declared

10. Matthias Stöck

    Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB, Berlin, Germany

    Contribution

    Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-4888-8371

11. Dmitrij Dedukh

    Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CAS, Libechov, Czech Republic

    Contribution

    Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

    For correspondence

    dmitrijdedukh@gmail.com

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-1152-813X

12. Karel Janko

    1. Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CAS, Libechov, Czech Republic
    2. Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic

    Contribution

    Data curation, Formal analysis, Funding acquisition, Project administration, Writing – review and editing, Supervision

    For correspondence

    janko@iapg.cas.cz

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-7866-4937

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