Asexual Reproduction Does Not Apparently Increase the Rate of Chromosomal Evolution: Karyotype Stability in Diploid and Triploid Clonal Hybrid Fish (Cobitis, Cypriniformes, Teleostei)

Majtánová, Zuzana; Choleva, Lukáš; Symonová, Radka; Ráb, Petr; Kotusz, Jan; Pekárik, Ladislav; Janko, Karel

doi:10.1371/journal.pone.0146872

Cited by 42 publications

(57 citation statements)

References 67 publications

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“…Extensive crossing experiments have never documented allelic segregation (Choleva et al., 2012; Janko, Bohlen, et al, 2007; Janko et al., 2018), and Majtánová et al. (2016) reported remarkable stability of the hybrids’ karyotypes with no large‐scale chromosomal restructuring or recombination. The current study also shows that the vast majority of the private hybrid SNPs occur in heterozygous states (between 98.5% and 99.8%), which corroborates the hypothesized clonal reproduction, with new mutations occurring on one chromosome with little possibility of recombination between the homologues or coalescence between the alleles.…”

Section: Discussionmentioning

confidence: 99%

No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets

et al. 2020

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Despite its inherent costs, sexual reproduction is ubiquitous in nature, and the mechanisms to protect it from a competitive displacement by asexuality remain unclear. Popular mutation‐based explanations, like the Muller's ratchet and the Kondrashov's hatchet, assume that purifying selection may not halt the accumulation of deleterious mutations in the nonrecombining genomes, ultimately leading to their degeneration. However, empirical evidence is scarce and it remains particularly unclear whether mutational degradation proceeds fast enough to ensure the decay of clonal organisms and to prevent them from outcompeting their sexual counterparts. To test this hypothesis, we jointly analysed the exome sequences and the fitness‐related phenotypic traits of the sexually reproducing fish species and their clonal hybrids, whose evolutionary ages ranged from F1 generations to 300 ky. As expected, mutations tended to accumulate in the clonal genomes in a time‐dependent manner. However, contrary to the predictions, we found no trend towards increased nonsynonymity of mutations acquired by clones, nor higher radicality of their amino acid substitutions. Moreover, there was no evidence for fitness degeneration in the old clones compared with that in the younger ones. In summary, although an efficacy of purifying selection may still be reduced in the asexual genomes, our data indicate that its efficiency is not drastically decreased. Even the oldest investigated clone was found to be too young to suffer fitness consequences from a mutation accumulation. This suggests that mechanisms other than mutation accumulation may be needed to explain the competitive advantage of sex in the short term.

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Section: Discussionmentioning

confidence: 99%

No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets

et al. 2020

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“…PNA probe for TTAGGG sequence was performed on metaphase slides and slides with male pachytene chromosomes according to the protocol provided by manufacturer (DAKO). Comparative genome hybridization (CGH) was made according to [56] on the same slides where telomeric sites were detected by FISH. Detail description of CGH is given in S1 Methods.…”

Section: Fluorescent In Situ Hybridization and Comparative Genomic Hymentioning

confidence: 99%

Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Dedukh

Majtánová

Marta

et al. 2019

Preprint

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Formation of species generally occurs in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report that speciation proceeds through a previously unnoticed stage at which gene flow is completely interrupted on side of both hybrid's sexes, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to the formation of clonal gametes. Specifically, analysis of gametogenetic pathways in hybrids between fish species Cobitis elongatoides and C. taenia revealed that male HS resulted from extensive asynapses and crossover reduction among elongatoides-taenia chromosomal pairs followed by apoptosis. By contrast, hybrid females exhibited premeiotic genome endoreplication which ensured proper formation of bivalents between identical chromosomal copies. This deviation ultimately restored fertility in females but since it simultaneously leads to the production of unreduced clonal gametes, it restricts interspecific gene flow thereby directly contributing to speciation. In conclusion, our data demonstrate that the emergence of asexuality may remedy HS in a sex-specific manner and is intermingled with the speciation process. Although gametogenetic mechanisms employed by asexual animals and plants have rarely been scrutinized, available evidence suggests that premeiotic endoreplication is relatively widespread. This suggests that observed link between HS and clonality may have general validity in taxa able of asexual reproduction. Author's summarySpecies are fundamental evolutionary units that presumably evolve in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report the existence of a previously unnoticed stage of speciation at which gene flow is completely interrupted, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to formation of clonal gametes. Specifically, HS resulted from extensive asynapses in male gonads, but in females the hybridization provoked premeiotic endoreplication which rescued chromosome pairing and fertility. Simultaneously, this meiotic deviation caused clonal transmission of maternal genome, thereby effectively restricting the interspeficic gene flow. Our results emphasize that emergence of clonality is a type of hybrid incompatibility that is intermingled with the formation of b...

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“…Thirdly, we estimated levels and timing of historical gene flow among the species by analysed single nucleotide polymorphisms (SNP) variability of C. elongatoides, C. taenia, C. tanaitica and C. pontica transcriptomes. As an outgroup we used C. strumicae -a species belonging to subgenus Bicanestrinia whose divergence from the ingroup was set to 17.7 Mya according to [35], which was sampled in isolated Black Sea tributaries outside of the distribution ranges of ingroup species in order to avoid any possible reproductive contact. The assembly of mRNA from five C. taenia specimens comprised 20,385 contigs (potential mRNAs) and was used as a reference for mapping of reads from all species (two individuals of each ingroup species and one outgroup).…”

Section: Estimation Of Levels and Timing Of Historical Gene Flow Amonmentioning

confidence: 99%

“…The relative mutation rates at all loci were estimated by comparison with an outgroup species [76]. C. strumicae was used as outgroup, whose divergence time from the ingroup was set to 17.7 Mya according to the penalized likelihood time-calibrated tree of [35]. Computation of 95% confidence intervals was based on the profile likelihood as described in [39].…”

Section: Detection Of Historical Admixturementioning

confidence: 99%

Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

Janko

Pačes

Wilkinson‐Herbots

et al. 2016

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Speciation usually proceeds in a continuum from intensively hybridizing populations until the formation of irreversibly isolated species. Restriction of interspecific gene flow may often be achieved by gradual accumulation of intrinsic postzygotic incompatibilities with hybrid infertility typically evolving more rapidly than inviability. A reconstructed history of speciation in European loaches (Cobitis) reveals that accumulation of postzygotic reproductive incompatibilities may take an alternative, in the literature largely neglected, pathway through initiation of hybrids' asexuality rather than through a decrease in hybrids' fitness. Combined evidence shows that contemporary Cobitis species readily hybridize in hybrid zones, but their gene pools are isolated as hybridization produces infertile males and fertile but clonally reproducing females that cannot mediate introgressions. Nevertheless, coalescent analyses indicated intensive historical gene flow during earlier stages of Cobitis diversification, suggesting that non-clonal hybrids must have existed in the past. The revealed patterns imply that during the initial stages of speciation, hybridization between little diverged species produced recombinant hybrids mediating gene flow, but growing divergence among species caused disrupted meiosis in hybrids resulting in their clonality, which acts as a barrier to gene flow. Comparative analysis of published data on other fish hybrids corroborated the generality of our findings; the species pairs producing asexual hybrids were more genetically diverged than those pairs producing fertile sexual hybrids but less diverged than species pairs producing infertile hybrids. Hybrid asexuality therefore appears to evolve at lower divergence than other types of postzygotic barriers and might thus represent a primary reproductive barrier in many taxa.

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Asexual Reproduction Does Not Apparently Increase the Rate of Chromosomal Evolution: Karyotype Stability in Diploid and Triploid Clonal Hybrid Fish (Cobitis, Cypriniformes, Teleostei)

Cited by 42 publications

References 67 publications

No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets

No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets

Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

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