Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions
Abstract Background Sexually dimorphic mating behaviors differ between sexes and involve gonadal hormones and possibly sexually dimorphic gene expression in the brain. However, the associations among the brain, gonad, and sexual behavior in teleosts are still unclear. Here, we utilized germ cells-fr...
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| Format: | Article |
| Language: | English |
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BMC
2023-08-01
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| Series: | Biology of Sex Differences |
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| Online Access: | https://doi.org/10.1186/s13293-023-00534-7 |
| _version_ | 1827635824903061504 |
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| author | Xiangyan Dai Ajay Pradhan Jiao Liu Ruolan Liu Gang Zhai Linyan Zhou Jiyan Dai Feng Shao Zhiyong Yuan Zhijian Wang Zhan Yin |
| author_facet | Xiangyan Dai Ajay Pradhan Jiao Liu Ruolan Liu Gang Zhai Linyan Zhou Jiyan Dai Feng Shao Zhiyong Yuan Zhijian Wang Zhan Yin |
| author_sort | Xiangyan Dai |
| collection | DOAJ |
| description | Abstract Background Sexually dimorphic mating behaviors differ between sexes and involve gonadal hormones and possibly sexually dimorphic gene expression in the brain. However, the associations among the brain, gonad, and sexual behavior in teleosts are still unclear. Here, we utilized germ cells-free tdrd12 knockout (KO) zebrafish, and steroid synthesis enzyme cyp17a1-deficient zebrafish to investigate the differences and interplays in the brain–gonad–behavior axis, and the molecular control of brain dimorphism and male mating behaviors. Methods Tdrd12 +/−; cyp17a1 +/− double heterozygous parents were crossed to obtain tdrd12 −/− ; cyp17a1 +/+ (tdrd12 KO), tdrd12 +/+; cyp17a1 −/− (cyp17a1 KO), and tdrd12 −/− ; cyp17a1 −/− (double KO) homozygous progenies. Comparative analysis of mating behaviors were evaluated using Viewpoint zebrafish tracking software and sexual traits were thoroughly characterized based on anatomical and histological experiments in these KOs and wild types. The steroid hormone levels (testosterone, 11-ketotestosterone and 17β-estradiol) in the brains, gonads, and serum were measured using ELISA kits. To achieve a higher resolution view of the differences in region-specific expression patterns of the brain, the brains of these KOs, and control male and female fish were dissected into three regions: the forebrain, midbrain, and hindbrain for transcriptomic analysis. Results Qualitative analysis of mating behaviors demonstrated that tdrd12 −/− fish behaved in the same manner as wild-type males to trigger oviposition behavior, while cyp17a1 −/− and double knockout (KO) fish did not exhibit these behaviors. Based on the observation of sex characteristics, mating behaviors and hormone levels in these mutants, we found that the maintenance of secondary sex characteristics and male mating behavior did not depend on the presence of germ cells; rather, they depended mainly on the 11-ketotestosterone and testosterone levels secreted into the brain–gonad regulatory axis. RNA-seq analysis of different brain regions revealed that the brain transcript profile of tdrd12 −/− fish was similar to that of wild-type males, especially in the forebrain and midbrain. However, the brain transcript profiles of cyp17a1 −/− and double KO fish were distinct from those of wild-type males and were partially biased towards the expression pattern of the female brain. Our results revealed important candidate genes and signaling pathways, such as synaptic signaling/neurotransmission, MAPK signaling, and steroid hormone pathways, that shape brain dimorphism and modulate male mating behavior in zebrafish. Conclusions Our results provide comprehensive analyses and new insights regarding the endogenous interactions in the brain–gonad–behavior axis. Moreover, this study revealed the crucial candidate genes and neural signaling pathways of different brain regions that are involved in modulating brain dimorphism and male mating behavior in zebrafish, which would significantly light up the understanding the neuroendocrine and molecular mechanisms modulating brain dimorphism and male mating behavior in zebrafish and other teleost fish. Graphical Abstract |
| first_indexed | 2024-03-09T15:31:53Z |
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| institution | Directory Open Access Journal |
| issn | 2042-6410 |
| language | English |
| last_indexed | 2024-03-09T15:31:53Z |
| publishDate | 2023-08-01 |
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| series | Biology of Sex Differences |
| spelling | doaj.art-21c10641c9db4d3e925951f45405f33a2023-11-26T12:09:50ZengBMCBiology of Sex Differences2042-64102023-08-0114111610.1186/s13293-023-00534-7Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regionsXiangyan Dai0Ajay Pradhan1Jiao Liu2Ruolan Liu3Gang Zhai4Linyan Zhou5Jiyan Dai6Feng Shao7Zhiyong Yuan8Zhijian Wang9Zhan Yin10Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityBiology, The Life Science Center, School of Science and Technology, Örebrorebro UniversityKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest UniversityState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesAbstract Background Sexually dimorphic mating behaviors differ between sexes and involve gonadal hormones and possibly sexually dimorphic gene expression in the brain. However, the associations among the brain, gonad, and sexual behavior in teleosts are still unclear. Here, we utilized germ cells-free tdrd12 knockout (KO) zebrafish, and steroid synthesis enzyme cyp17a1-deficient zebrafish to investigate the differences and interplays in the brain–gonad–behavior axis, and the molecular control of brain dimorphism and male mating behaviors. Methods Tdrd12 +/−; cyp17a1 +/− double heterozygous parents were crossed to obtain tdrd12 −/− ; cyp17a1 +/+ (tdrd12 KO), tdrd12 +/+; cyp17a1 −/− (cyp17a1 KO), and tdrd12 −/− ; cyp17a1 −/− (double KO) homozygous progenies. Comparative analysis of mating behaviors were evaluated using Viewpoint zebrafish tracking software and sexual traits were thoroughly characterized based on anatomical and histological experiments in these KOs and wild types. The steroid hormone levels (testosterone, 11-ketotestosterone and 17β-estradiol) in the brains, gonads, and serum were measured using ELISA kits. To achieve a higher resolution view of the differences in region-specific expression patterns of the brain, the brains of these KOs, and control male and female fish were dissected into three regions: the forebrain, midbrain, and hindbrain for transcriptomic analysis. Results Qualitative analysis of mating behaviors demonstrated that tdrd12 −/− fish behaved in the same manner as wild-type males to trigger oviposition behavior, while cyp17a1 −/− and double knockout (KO) fish did not exhibit these behaviors. Based on the observation of sex characteristics, mating behaviors and hormone levels in these mutants, we found that the maintenance of secondary sex characteristics and male mating behavior did not depend on the presence of germ cells; rather, they depended mainly on the 11-ketotestosterone and testosterone levels secreted into the brain–gonad regulatory axis. RNA-seq analysis of different brain regions revealed that the brain transcript profile of tdrd12 −/− fish was similar to that of wild-type males, especially in the forebrain and midbrain. However, the brain transcript profiles of cyp17a1 −/− and double KO fish were distinct from those of wild-type males and were partially biased towards the expression pattern of the female brain. Our results revealed important candidate genes and signaling pathways, such as synaptic signaling/neurotransmission, MAPK signaling, and steroid hormone pathways, that shape brain dimorphism and modulate male mating behavior in zebrafish. Conclusions Our results provide comprehensive analyses and new insights regarding the endogenous interactions in the brain–gonad–behavior axis. Moreover, this study revealed the crucial candidate genes and neural signaling pathways of different brain regions that are involved in modulating brain dimorphism and male mating behavior in zebrafish, which would significantly light up the understanding the neuroendocrine and molecular mechanisms modulating brain dimorphism and male mating behavior in zebrafish and other teleost fish. Graphical Abstracthttps://doi.org/10.1186/s13293-023-00534-7Mating behaviorsSex characteristicsHormonesBrain dimorphismBrain transcriptomesZebrafish |
| spellingShingle | Xiangyan Dai Ajay Pradhan Jiao Liu Ruolan Liu Gang Zhai Linyan Zhou Jiyan Dai Feng Shao Zhiyong Yuan Zhijian Wang Zhan Yin Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions Biology of Sex Differences Mating behaviors Sex characteristics Hormones Brain dimorphism Brain transcriptomes Zebrafish |
| title | Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| title_full | Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| title_fullStr | Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| title_full_unstemmed | Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| title_short | Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| title_sort | zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions |
| topic | Mating behaviors Sex characteristics Hormones Brain dimorphism Brain transcriptomes Zebrafish |
| url | https://doi.org/10.1186/s13293-023-00534-7 |
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