Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex

The transition from sexual reproduction to asexuality is often triggered by hybridization. The gametogenesis of many hybrid asexuals involves premeiotic genome endoreplication leading to bypass hybrid sterility and forming clonal gametes. However, it is still not clear when endoreplication occurs, h...

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Main Authors: Dmitrij Dedukh, Anatolie Marta, Karel Janko
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/22/12117
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author Dmitrij Dedukh
Anatolie Marta
Karel Janko
author_facet Dmitrij Dedukh
Anatolie Marta
Karel Janko
author_sort Dmitrij Dedukh
collection DOAJ
description The transition from sexual reproduction to asexuality is often triggered by hybridization. The gametogenesis of many hybrid asexuals involves premeiotic genome endoreplication leading to bypass hybrid sterility and forming clonal gametes. However, it is still not clear when endoreplication occurs, how many gonial cells it affects and whether its rate differs among clonal lineages. Here, we investigated meiotic and premeiotic cells of diploid and triploid hybrids of spined loaches (Cypriniformes: <i>Cobitis</i>) that reproduce by gynogenesis. We found that in naturally and experimentally produced F1 hybrids asexuality is achieved by genome endoreplication, which occurs in gonocytes just before entering meiosis or, rarely, one or a few divisions before meiosis. However, genome endoreplication was observed only in a minor fraction of the hybrid’s gonocytes, while the vast majority of gonocytes were unable to duplicate their genomes and consequently could not proceed beyond pachytene due to defects in bivalent formation. We also noted that the rate of endoreplication was significantly higher among gonocytes of hybrids from natural clones than of experimentally produced F1 hybrids. Thus, asexuality and hybrid sterility are intimately related phenomena and the transition from sexual reproduction to asexuality must overcome significant problems with genome incompatibilities with a possible impact on reproductive potential.
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spelling doaj.art-2cc5211edafd4bb08e3278c2c5ddfe032023-11-22T23:37:32ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-11-0122221211710.3390/ijms222212117Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> ComplexDmitrij Dedukh0Anatolie Marta1Karel Janko2Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics of the CAS, Rumburská 89, 277 21 Liběchov, Czech RepublicLaboratory of Fish Genetics, Institute of Animal Physiology and Genetics of the CAS, Rumburská 89, 277 21 Liběchov, Czech RepublicLaboratory of Fish Genetics, Institute of Animal Physiology and Genetics of the CAS, Rumburská 89, 277 21 Liběchov, Czech RepublicThe transition from sexual reproduction to asexuality is often triggered by hybridization. The gametogenesis of many hybrid asexuals involves premeiotic genome endoreplication leading to bypass hybrid sterility and forming clonal gametes. However, it is still not clear when endoreplication occurs, how many gonial cells it affects and whether its rate differs among clonal lineages. Here, we investigated meiotic and premeiotic cells of diploid and triploid hybrids of spined loaches (Cypriniformes: <i>Cobitis</i>) that reproduce by gynogenesis. We found that in naturally and experimentally produced F1 hybrids asexuality is achieved by genome endoreplication, which occurs in gonocytes just before entering meiosis or, rarely, one or a few divisions before meiosis. However, genome endoreplication was observed only in a minor fraction of the hybrid’s gonocytes, while the vast majority of gonocytes were unable to duplicate their genomes and consequently could not proceed beyond pachytene due to defects in bivalent formation. We also noted that the rate of endoreplication was significantly higher among gonocytes of hybrids from natural clones than of experimentally produced F1 hybrids. Thus, asexuality and hybrid sterility are intimately related phenomena and the transition from sexual reproduction to asexuality must overcome significant problems with genome incompatibilities with a possible impact on reproductive potential.https://www.mdpi.com/1422-0067/22/22/12117gynogenesismeiosishybrid sterilityendoreplicationpolyploidy<i>Cobitis taenia</i> complex
spellingShingle Dmitrij Dedukh
Anatolie Marta
Karel Janko
Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
International Journal of Molecular Sciences
gynogenesis
meiosis
hybrid sterility
endoreplication
polyploidy
<i>Cobitis taenia</i> complex
title Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
title_full Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
title_fullStr Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
title_full_unstemmed Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
title_short Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from <i>Cobitis taenia</i> Complex
title_sort challenges and costs of asexuality variation in premeiotic genome duplication in gynogenetic hybrids from i cobitis taenia i complex
topic gynogenesis
meiosis
hybrid sterility
endoreplication
polyploidy
<i>Cobitis taenia</i> complex
url https://www.mdpi.com/1422-0067/22/22/12117
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AT anatoliemarta challengesandcostsofasexualityvariationinpremeioticgenomeduplicationingynogenetichybridsfromicobitistaeniaicomplex
AT kareljanko challengesandcostsofasexualityvariationinpremeioticgenomeduplicationingynogenetichybridsfromicobitistaeniaicomplex