High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity

Recently, concerns for species that sex differentiation is influenced by temperature in the context of global warming have increased because disrupted operational sex ratios could threaten population maintenance. In contrast, little attention has been given to the reproductive ability of populations...

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Main Authors: Yue Yu, Min Chen, Zi-Yi Lu, Ya Liu, Bo Li, Ze-Xia Gao, Zhi-Gang Shen
Format: Article
Language:English
Published: Elsevier 2022-07-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S014765132200478X
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author Yue Yu
Min Chen
Zi-Yi Lu
Ya Liu
Bo Li
Ze-Xia Gao
Zhi-Gang Shen
author_facet Yue Yu
Min Chen
Zi-Yi Lu
Ya Liu
Bo Li
Ze-Xia Gao
Zhi-Gang Shen
author_sort Yue Yu
collection DOAJ
description Recently, concerns for species that sex differentiation is influenced by temperature in the context of global warming have increased because disrupted operational sex ratios could threaten population maintenance. In contrast, little attention has been given to the reproductive ability of populations that experienced elevated temperatures. In this study, we demonstrated that high temperature (HT) would decrease population size via three different aspects of reproductive ability for the first time. We show that, in a thermo-sensitive teleost yellow catfish, a short period of HT (+3 °C) exposure during the critical period of sex differentiation leads to a different percentage of masculinization of XX genotypic females (1–23%) in wet-lab and natural water bodies. Combining the results of gonadal appearance, histology, sperm parameters, and fertilization rate, we found that XX pseudo-males induced by HT display significantly discounted fertility and reproductive performance compared to XY normal males. We demonstrate that the survival of the XY genotype is lower than XX genotype under environmental stress, including HT, hypoxia, and parasite infection, and the differential survival seems unrelated to male-biased sexual size dimorphism. The mathematical model predicts that the phenotypic female percent will be stabilized at 50% and the population will be sustainably maintained when masculinizing force is less than 0.5, while HT will put the population in danger when the masculinizing force exceeds 0.5. However, when we combine the real-world data of reproductive ability and mathematic model, our results suggest the population size decreases and the long-term survival of the studied species are threatened under the projected pace of increasing temperature. These findings will be useful for understanding the long-term effects of increasing temperature on sex ratio, reproduction and population maintenance in teleost.
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spelling doaj.art-93385d3a815c4c9f835654e6d11eeb942022-12-22T02:27:28ZengElsevierEcotoxicology and Environmental Safety0147-65132022-07-01239113638High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivityYue Yu0Min Chen1Zi-Yi Lu2Ya Liu3Bo Li4Ze-Xia Gao5Zhi-Gang Shen6College of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR ChinaCollege of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR ChinaCollege of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR ChinaCollege of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR ChinaInstitute of Fisheries, Wuhan Academy of Agricultural Sciences, Wuhan, PR ChinaCollege of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR ChinaCollege of Fisheries, Engineering Research Center of Green development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Huazhong Agricultural University, Wuhan, PR China; Correspondence to: College of Fisheries, Huazhong Agricultural University, Hongshan District, Wuhan 430070, PR China.Recently, concerns for species that sex differentiation is influenced by temperature in the context of global warming have increased because disrupted operational sex ratios could threaten population maintenance. In contrast, little attention has been given to the reproductive ability of populations that experienced elevated temperatures. In this study, we demonstrated that high temperature (HT) would decrease population size via three different aspects of reproductive ability for the first time. We show that, in a thermo-sensitive teleost yellow catfish, a short period of HT (+3 °C) exposure during the critical period of sex differentiation leads to a different percentage of masculinization of XX genotypic females (1–23%) in wet-lab and natural water bodies. Combining the results of gonadal appearance, histology, sperm parameters, and fertilization rate, we found that XX pseudo-males induced by HT display significantly discounted fertility and reproductive performance compared to XY normal males. We demonstrate that the survival of the XY genotype is lower than XX genotype under environmental stress, including HT, hypoxia, and parasite infection, and the differential survival seems unrelated to male-biased sexual size dimorphism. The mathematical model predicts that the phenotypic female percent will be stabilized at 50% and the population will be sustainably maintained when masculinizing force is less than 0.5, while HT will put the population in danger when the masculinizing force exceeds 0.5. However, when we combine the real-world data of reproductive ability and mathematic model, our results suggest the population size decreases and the long-term survival of the studied species are threatened under the projected pace of increasing temperature. These findings will be useful for understanding the long-term effects of increasing temperature on sex ratio, reproduction and population maintenance in teleost.http://www.sciencedirect.com/science/article/pii/S014765132200478XTemperature sex determinationSex differentiationClimate changeEnvironmental stressMasculinizationSex-specific mortality
spellingShingle Yue Yu
Min Chen
Zi-Yi Lu
Ya Liu
Bo Li
Ze-Xia Gao
Zhi-Gang Shen
High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
Ecotoxicology and Environmental Safety
Temperature sex determination
Sex differentiation
Climate change
Environmental stress
Masculinization
Sex-specific mortality
title High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
title_full High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
title_fullStr High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
title_full_unstemmed High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
title_short High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
title_sort high temperature stress will put the thermo sensitive teleost yellow catfish tachysurus fulvidraco in danger through reducing reproductivity
topic Temperature sex determination
Sex differentiation
Climate change
Environmental stress
Masculinization
Sex-specific mortality
url http://www.sciencedirect.com/science/article/pii/S014765132200478X
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