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      A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level

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          Abstract

          The cellular and molecular mechanisms governing sexual reproduction are conserved across eukaryotes. Nevertheless, hybridization can disrupt these mechanisms, leading to asexual reproduction, often accompanied by polyploidy. In this study, we investigate how ploidy level and ratio of parental genomes in hybrids affect their reproductive mode. We analyze the gametogenesis of sexual species and their diploid and triploid hybrids from the freshwater fish family Cobitidae, using newly developed cytogenetic markers. We find that diploid hybrid females possess oogonia and oocytes with original (diploid) and duplicated (tetraploid) ploidy. Diploid oocytes cannot progress beyond pachytene due to aberrant pairing. However, tetraploid oocytes, which emerge after premeiotic genome endoreplication, exhibit normal pairing and result in diploid gametes. Triploid hybrid females possess diploid, triploid, and haploid oogonia and oocytes. Triploid and haploid oocytes cannot progress beyond pachytene checkpoint due to aberrant chromosome pairing, while diploid oocytes have normal pairing in meiosis, resulting in haploid gametes. Diploid oocytes emerge after premeiotic elimination of a single-copied genome. Triploid hybrid males are sterile due to aberrant pairing and the failure of chromosomal segregation during meiotic divisions. Thus, changes in ploidy and genome dosage may lead to cyclical alteration of gametogenic pathways in hybrids.

          Abstract

          The cytogenetic analysis of gonial cells and meiocytes on Korean loach complex suggest that instant switch between sexual to asexual reproduction in hybrids depend on their ploidy and genome dosage.

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          Most cited references73

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            Resolving the paradox of sex and recombination.

            Sexual reproduction and recombination are ubiquitous. However, a large body of theoretical work has shown that these processes should only evolve under a restricted set of conditions. New studies indicate that this discrepancy might result from the fact that previous models have ignored important complexities that face natural populations, such as genetic drift and the spatial structure of populations.
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              Chromosomal rearrangements and speciation.

              Several authors have proposed that speciation frequently occurs when a population becomes fixed for one or more chromosomal rearrangements that reduce fitness when they are heterozygous. This hypothesis has little theoretical support because mutations that cause a large reduction in fitness can be fixed through drift only in small, inbred populations. Moreover, the effects of chromosomal rearrangements on fitness are unpredictable and vary significantly between plants and animals. I argue that rearrangements reduce gene flow more by suppressing recombination and extending the effects of linked isolation genes than by reducing fitness. This unorthodox perspective has significant implications for speciation models and for the outcomes of contact between neospecies and their progenitor(s).
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                Author and article information

                Contributors
                dmitrijdedukh@gmail.com
                Janko@iapg.cas.cz
                Journal
                Commun Biol
                Commun Biol
                Communications Biology
                Nature Publishing Group UK (London )
                2399-3642
                8 April 2024
                8 April 2024
                2024
                : 7
                : 424
                Affiliations
                [1 ]GRID grid.435109.a, ISNI 0000 0004 0639 4223, Laboratory of Non-Mendelian Evolution, , Institute of Animal Physiology and Genetics of the CAS, ; Liběchov, Czech Republic
                [2 ]Division of EcoScience, Ewha Womans University, ( https://ror.org/053fp5c05) Seoul, South Korea
                [3 ]Kosoo Ecology Institute, Seoul, South Korea
                [4 ]Department of Biology and Ecology, Faculty of Science, University of Ostrava, ( https://ror.org/00pyqav47) Ostrava, Czech Republic
                Author information
                http://orcid.org/0000-0002-1152-813X
                http://orcid.org/0000-0002-4457-8838
                http://orcid.org/0000-0002-7866-4937
                Article
                5948
                10.1038/s42003-024-05948-6
                11001910
                38589507
                05dfafdc-64a2-4396-9d78-1a21efd4e65b
                © The Author(s) 2024

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 July 2023
                : 21 February 2024
                Funding
                Funded by: Ministry of Education, Youth and Sports of the Czech Republic (grant no. 539 EXCELLENCE CZ.02.1.01/0.0/0.0/15_003/0000460 OP RDE) Institutional Research Concept RVO67985904
                Funded by: FundRef https://doi.org/10.13039/501100001824, Grantová Agentura České Republiky (Grant Agency of the Czech Republic);
                Award ID: 21-25185S
                Award ID: 21-25185S
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100003725, National Research Foundation of Korea (NRF);
                Award ID: 2015R1A2A2A01007117 and 2019R1I1A2A02057134
                Award Recipient :
                Categories
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                © Springer Nature Limited 2024

                cytogenetics,evolutionary biology,germline development

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