Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus
Abstract Gametogenesis produces gametes as a piece of genetic information transmitted to the offspring. While during sexual reproduction, progeny inherits a mix of genetic material from both parents, asexually reproducing organisms transfer a copy of maternal or paternal DNA to the progeny clonally....
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Nature Portfolio
2024-09-01
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| Online Access: | https://doi.org/10.1038/s41598-024-73043-1 |
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| author | Marie Doležálková-Kaštánková Dmitrij Dedukh Veronika Labajová Eleonora Pustovalova Lukáš Choleva |
| author_facet | Marie Doležálková-Kaštánková Dmitrij Dedukh Veronika Labajová Eleonora Pustovalova Lukáš Choleva |
| author_sort | Marie Doležálková-Kaštánková |
| collection | DOAJ |
| description | Abstract Gametogenesis produces gametes as a piece of genetic information transmitted to the offspring. While during sexual reproduction, progeny inherits a mix of genetic material from both parents, asexually reproducing organisms transfer a copy of maternal or paternal DNA to the progeny clonally. Parthenogenetic, gynogenetic and hybridogenetic animals have developed various mechanisms of gametogenesis, however, their inheritance is not fully understood. Here, we focused on the inheritance of asexual gametogenesis in hybrid Pelophylax esculentus (RL), emerging after crosses of P. lessonae (LL) and P. ridibundus (RR). To understand the mechanisms of gametogenesis in hybrids, we performed three-generation experiments of sexual P. ridibundus females and hybrids from all-male hybrid populations. Using fluorescent in situ hybridization, micronuclei analysis, flow cytometry and genotyping, we found that most adult hybrid males simultaneously produced two types of clonal sperm. Also, most male tadpole progeny in two successive backcrossed generations simultaneously eliminated L and R parental genomes, while some progeny produced only one type of sperm. We hypothesize that the reproductive variability of males producing two kinds of sperm is an adaptive mechanism to reproduce in mixed populations with P. ridibundus and may explain the extensive distribution of the all-male lineage across the European River Basin. |
| format | Article |
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| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2024-09-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-2e4d0e086a6647eba5f9619ce8db2ff12025-01-19T12:24:57ZengNature PortfolioScientific Reports2045-23222024-09-0114111510.1038/s41598-024-73043-1Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentusMarie Doležálková-Kaštánková0Dmitrij Dedukh1Veronika Labajová2Eleonora Pustovalova3Lukáš Choleva4Institute of Animal Physiology and Genetics, Laboratory of NonMendelian Evolution, The Czech Academy of SciencesInstitute of Animal Physiology and Genetics, Laboratory of NonMendelian Evolution, The Czech Academy of SciencesDepartment of Biology and Ecology, Faculty of Science, University of OstravaInstitute of Animal Physiology and Genetics, Laboratory of Fish Genetics, The Czech Academy of SciencesDepartment of Biology and Ecology, Faculty of Science, University of OstravaAbstract Gametogenesis produces gametes as a piece of genetic information transmitted to the offspring. While during sexual reproduction, progeny inherits a mix of genetic material from both parents, asexually reproducing organisms transfer a copy of maternal or paternal DNA to the progeny clonally. Parthenogenetic, gynogenetic and hybridogenetic animals have developed various mechanisms of gametogenesis, however, their inheritance is not fully understood. Here, we focused on the inheritance of asexual gametogenesis in hybrid Pelophylax esculentus (RL), emerging after crosses of P. lessonae (LL) and P. ridibundus (RR). To understand the mechanisms of gametogenesis in hybrids, we performed three-generation experiments of sexual P. ridibundus females and hybrids from all-male hybrid populations. Using fluorescent in situ hybridization, micronuclei analysis, flow cytometry and genotyping, we found that most adult hybrid males simultaneously produced two types of clonal sperm. Also, most male tadpole progeny in two successive backcrossed generations simultaneously eliminated L and R parental genomes, while some progeny produced only one type of sperm. We hypothesize that the reproductive variability of males producing two kinds of sperm is an adaptive mechanism to reproduce in mixed populations with P. ridibundus and may explain the extensive distribution of the all-male lineage across the European River Basin.https://doi.org/10.1038/s41598-024-73043-1Crossing experimentsSpermatogenesisMale hybridogenesisMonospermicAmphispermyMicronuclei |
| spellingShingle | Marie Doležálková-Kaštánková Dmitrij Dedukh Veronika Labajová Eleonora Pustovalova Lukáš Choleva Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus Scientific Reports Crossing experiments Spermatogenesis Male hybridogenesis Monospermic Amphispermy Micronuclei |
| title | Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus |
| title_full | Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus |
| title_fullStr | Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus |
| title_full_unstemmed | Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus |
| title_short | Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus |
| title_sort | inheritance patterns of male asexuality in hybrid males of a water frog pelophylax esculentus |
| topic | Crossing experiments Spermatogenesis Male hybridogenesis Monospermic Amphispermy Micronuclei |
| url | https://doi.org/10.1038/s41598-024-73043-1 |
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