Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)

Abstract Obligatory parthenogenesis in vertebrates is restricted to squamate reptiles and evolved through hybridisation. Parthenogens can hybridise with sexual species, resulting in individuals with increased ploidy levels. We describe two successive hybridisations of the parthenogenetic butterfly l...

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Main Authors: Eduard Galoyan, Roman Nazarov, Marie Altmanová, Sergey Matveevsky, Ivan Kropachev, Dmitrij Dedukh, Eugene Iryshkov, Mark Pankin, Natalia Sopilko, Oleg Nikolaev, Nikolai Orlov, Marine Arakelyan, Jiří Klíma, Evgeniya Solovyeva, Tao Nguyen, Lukáš Kratochvíl
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-83300-y
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author Eduard Galoyan
Roman Nazarov
Marie Altmanová
Sergey Matveevsky
Ivan Kropachev
Dmitrij Dedukh
Eugene Iryshkov
Mark Pankin
Natalia Sopilko
Oleg Nikolaev
Nikolai Orlov
Marine Arakelyan
Jiří Klíma
Evgeniya Solovyeva
Tao Nguyen
Lukáš Kratochvíl
author_facet Eduard Galoyan
Roman Nazarov
Marie Altmanová
Sergey Matveevsky
Ivan Kropachev
Dmitrij Dedukh
Eugene Iryshkov
Mark Pankin
Natalia Sopilko
Oleg Nikolaev
Nikolai Orlov
Marine Arakelyan
Jiří Klíma
Evgeniya Solovyeva
Tao Nguyen
Lukáš Kratochvíl
author_sort Eduard Galoyan
collection DOAJ
description Abstract Obligatory parthenogenesis in vertebrates is restricted to squamate reptiles and evolved through hybridisation. Parthenogens can hybridise with sexual species, resulting in individuals with increased ploidy levels. We describe two successive hybridisations of the parthenogenetic butterfly lizards (genus Leiolepis) in Vietnam with a parental sexual species. Contrary to previous proposals, we document that parthenogenetic L. guentherpetersi has mitochondrial DNA and two haploid sets from L. guttata and one from L. reevesii, suggesting that it is the result of a backcross of a parthenogenetic L. guttata × L. reevesii hybrid with a L. guttata male increasing ploidy from 2n to 3n. Within the range of L. guentherpetersi, we found an adult tetraploid male with three L. guttata and one L. reevesii haploid genomes. It probably originated from fertilisation of an unreduced triploid L. guentherpetersi egg by a L. guttata sperm. Although its external morphology resembles that of the maternal species, it possessed exceptionally large erythrocytes and was likely sterile. As increased ploidy level above triploidy or tetraploidy appears to be harmful for amniotes, all-female asexual lineages should evolve a strategy to prevent incorporation of other haploid genomes from a sexual species by avoiding fertilisation by sexual males.
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spelling doaj-art-c3468b48065648789818b4f507b9e09d2025-01-26T12:28:03ZengNature PortfolioScientific Reports2045-23222025-01-0115111510.1038/s41598-024-83300-yNatural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)Eduard Galoyan0Roman Nazarov1Marie Altmanová2Sergey Matveevsky3Ivan Kropachev4Dmitrij Dedukh5Eugene Iryshkov6Mark Pankin7Natalia Sopilko8Oleg Nikolaev9Nikolai Orlov10Marine Arakelyan11Jiří Klíma12Evgeniya Solovyeva13Tao Nguyen14Lukáš Kratochvíl15Severtsov Institute of Ecology and Evolution of the Russian Academy of SciencesZoological Museum of Moscow State UniversityLaboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of SciencesVavilov Institute of General Genetics of the Russian Academy of SciencesSevertsov Institute of Ecology and Evolution of the Russian Academy of SciencesLaboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics, Czech Academy of SciencesSevertsov Institute of Ecology and Evolution of the Russian Academy of SciencesSevertsov Institute of Ecology and Evolution of the Russian Academy of SciencesSevertsov Institute of Ecology and Evolution of the Russian Academy of SciencesSevertsov Institute of Ecology and Evolution of the Russian Academy of SciencesZoological Institute, Russian Academy of SciencesDepartment of Zoology, Biological Faculty of Yerevan State UniversityLaboratory of Cell Regeneration and Plasticity, Institute of Animal Physiology and Genetics, Czech Academy of SciencesZoological Museum of Moscow State UniversityVietnam Academy of Science and TechnologyDepartment of Ecology, Faculty of Science, Charles UniversityAbstract Obligatory parthenogenesis in vertebrates is restricted to squamate reptiles and evolved through hybridisation. Parthenogens can hybridise with sexual species, resulting in individuals with increased ploidy levels. We describe two successive hybridisations of the parthenogenetic butterfly lizards (genus Leiolepis) in Vietnam with a parental sexual species. Contrary to previous proposals, we document that parthenogenetic L. guentherpetersi has mitochondrial DNA and two haploid sets from L. guttata and one from L. reevesii, suggesting that it is the result of a backcross of a parthenogenetic L. guttata × L. reevesii hybrid with a L. guttata male increasing ploidy from 2n to 3n. Within the range of L. guentherpetersi, we found an adult tetraploid male with three L. guttata and one L. reevesii haploid genomes. It probably originated from fertilisation of an unreduced triploid L. guentherpetersi egg by a L. guttata sperm. Although its external morphology resembles that of the maternal species, it possessed exceptionally large erythrocytes and was likely sterile. As increased ploidy level above triploidy or tetraploidy appears to be harmful for amniotes, all-female asexual lineages should evolve a strategy to prevent incorporation of other haploid genomes from a sexual species by avoiding fertilisation by sexual males.https://doi.org/10.1038/s41598-024-83300-yHybridisationLeiolepisParthenogenesisTetraploidyMeiosisVietnam
spellingShingle Eduard Galoyan
Roman Nazarov
Marie Altmanová
Sergey Matveevsky
Ivan Kropachev
Dmitrij Dedukh
Eugene Iryshkov
Mark Pankin
Natalia Sopilko
Oleg Nikolaev
Nikolai Orlov
Marine Arakelyan
Jiří Klíma
Evgeniya Solovyeva
Tao Nguyen
Lukáš Kratochvíl
Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
Scientific Reports
Hybridisation
Leiolepis
Parthenogenesis
Tetraploidy
Meiosis
Vietnam
title Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
title_full Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
title_fullStr Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
title_full_unstemmed Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
title_short Natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards (Leiolepis: Agamidae)
title_sort natural repeated backcrosses lead to triploidy and tetraploidy in parthenogenetic butterfly lizards leiolepis agamidae
topic Hybridisation
Leiolepis
Parthenogenesis
Tetraploidy
Meiosis
Vietnam
url https://doi.org/10.1038/s41598-024-83300-y
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