Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp
Unisexual lineages are commonly considered to be short-lived in the evolutionary process as accumulation of deleterious mutations stated by Muller’s ratchet. However, the gynogenetic hexaploid gibel carp (Carassius gibelio) with existence over 0.5 million years has wider ecological distribution and...
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Format: | Article |
Language: | English |
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Frontiers Media S.A.
2021-05-01
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Series: | Frontiers in Genetics |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fgene.2021.691923/full |
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Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Xin Zhao Xin Zhao Zhi Li Zhi Li Miao Ding Miao Ding Tao Wang Tao Wang Ming-Tao Wang Ming-Tao Wang Chun Miao Chun Miao Wen-Xuan Du Wen-Xuan Du Xiao-Juan Zhang Xiao-Juan Zhang Yang Wang Yang Wang Zhong-Wei Wang Zhong-Wei Wang Li Zhou Li Zhou Xi-Yin Li Xi-Yin Li Jian-Fang Gui Jian-Fang Gui |
spellingShingle |
Xin Zhao Xin Zhao Zhi Li Zhi Li Miao Ding Miao Ding Tao Wang Tao Wang Ming-Tao Wang Ming-Tao Wang Chun Miao Chun Miao Wen-Xuan Du Wen-Xuan Du Xiao-Juan Zhang Xiao-Juan Zhang Yang Wang Yang Wang Zhong-Wei Wang Zhong-Wei Wang Li Zhou Li Zhou Xi-Yin Li Xi-Yin Li Jian-Fang Gui Jian-Fang Gui Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp Frontiers in Genetics unisexual reproduction gynogenesis genetic diversity Muller’s ratchet genotypic sex determination temperature-dependent sex determination |
author_facet |
Xin Zhao Xin Zhao Zhi Li Zhi Li Miao Ding Miao Ding Tao Wang Tao Wang Ming-Tao Wang Ming-Tao Wang Chun Miao Chun Miao Wen-Xuan Du Wen-Xuan Du Xiao-Juan Zhang Xiao-Juan Zhang Yang Wang Yang Wang Zhong-Wei Wang Zhong-Wei Wang Li Zhou Li Zhou Xi-Yin Li Xi-Yin Li Jian-Fang Gui Jian-Fang Gui |
author_sort |
Xin Zhao |
title |
Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp |
title_short |
Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp |
title_full |
Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp |
title_fullStr |
Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp |
title_full_unstemmed |
Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp |
title_sort |
genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Genetics |
issn |
1664-8021 |
publishDate |
2021-05-01 |
description |
Unisexual lineages are commonly considered to be short-lived in the evolutionary process as accumulation of deleterious mutations stated by Muller’s ratchet. However, the gynogenetic hexaploid gibel carp (Carassius gibelio) with existence over 0.5 million years has wider ecological distribution and higher genetic diversity than its sexual progenitors, which provides an ideal model to investigate the underlying mechanisms on countering Muller’s ratchet in unisexual taxa. Unlike other unisexual lineages, the wild populations of gibel carp contain rare and variable proportions of males (1–26%), which are determined via two strategies including genotypic sex determination and temperature-dependent sex determination. Here, we used a maternal gibel carp from strain F to be mated with a genotypic male from strain A+, a temperature-dependent male from strain A+, and a male from another species common carp (Cyprinus carpio), respectively. When the maternal individual was mated with the genotypic male, a variant of gynogenesis was initiated, along with male occurrence, accumulation of microchromosomes, and creation of genetic diversity in the offspring. When the maternal individual was mated with the temperature-dependent male and common carp, typical gynogenesis was initiated that all the offspring showed the same genetic information as the maternal individual. Subsequently, we found out that the genotypic male nucleus swelled and contacted with the female nucleus after fertilization although it was extruded from the female nucleus eventually, which might be associated with the genetic variation in the offspring. These results reveal that genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp, which provides insights into the evolution of unisexual reproduction. |
topic |
unisexual reproduction gynogenesis genetic diversity Muller’s ratchet genotypic sex determination temperature-dependent sex determination |
url |
https://www.frontiersin.org/articles/10.3389/fgene.2021.691923/full |
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doaj-659c5d2f8daf44a38dcd20bb40726c582021-05-28T09:29:01ZengFrontiers Media S.A.Frontiers in Genetics1664-80212021-05-011210.3389/fgene.2021.691923691923Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel CarpXin Zhao0Xin Zhao1Zhi Li2Zhi Li3Miao Ding4Miao Ding5Tao Wang6Tao Wang7Ming-Tao Wang8Ming-Tao Wang9Chun Miao10Chun Miao11Wen-Xuan Du12Wen-Xuan Du13Xiao-Juan Zhang14Xiao-Juan Zhang15Yang Wang16Yang Wang17Zhong-Wei Wang18Zhong-Wei Wang19Li Zhou20Li Zhou21Xi-Yin Li22Xi-Yin Li23Jian-Fang Gui24Jian-Fang Gui25State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovative Academy of Seed Design, Hubei Hongshan Laboratory, Chinese Academy of Sciences, Wuhan, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaUnisexual lineages are commonly considered to be short-lived in the evolutionary process as accumulation of deleterious mutations stated by Muller’s ratchet. However, the gynogenetic hexaploid gibel carp (Carassius gibelio) with existence over 0.5 million years has wider ecological distribution and higher genetic diversity than its sexual progenitors, which provides an ideal model to investigate the underlying mechanisms on countering Muller’s ratchet in unisexual taxa. Unlike other unisexual lineages, the wild populations of gibel carp contain rare and variable proportions of males (1–26%), which are determined via two strategies including genotypic sex determination and temperature-dependent sex determination. Here, we used a maternal gibel carp from strain F to be mated with a genotypic male from strain A+, a temperature-dependent male from strain A+, and a male from another species common carp (Cyprinus carpio), respectively. When the maternal individual was mated with the genotypic male, a variant of gynogenesis was initiated, along with male occurrence, accumulation of microchromosomes, and creation of genetic diversity in the offspring. When the maternal individual was mated with the temperature-dependent male and common carp, typical gynogenesis was initiated that all the offspring showed the same genetic information as the maternal individual. Subsequently, we found out that the genotypic male nucleus swelled and contacted with the female nucleus after fertilization although it was extruded from the female nucleus eventually, which might be associated with the genetic variation in the offspring. These results reveal that genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp, which provides insights into the evolution of unisexual reproduction.https://www.frontiersin.org/articles/10.3389/fgene.2021.691923/fullunisexual reproductiongynogenesisgenetic diversityMuller’s ratchetgenotypic sex determinationtemperature-dependent sex determination |