Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination

Detalhes bibliográficos
Autor(a) principal: Valdivieso, Alejandro
Data de Publicação: 2022
Outros Autores: Wilson, Catherine A., Amores, Angel, da Silva Rodrigues, Maira [UNESP], Nóbrega, Rafael Henrique [UNESP], Ribas, Laia, Postlethwait, John H., Piferrer, Francesc
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1016/j.envres.2022.113549
http://hdl.handle.net/11449/241971
Resumo: Sex ratio depends on sex determination mechanisms and is a key demographic parameter determining population viability and resilience to natural and anthropogenic stressors. There is increasing evidence that the environment can alter sex ratio even in genetically sex-determined species (GSD), as elevated temperature can cause female-to-male sex reversal (neomales). Alarmingly, neomales are being discovered in natural populations of several fish, amphibian and reptile species worldwide. Understanding the basis of neomale development is important for conservation biology. Among GSD species, it is unknown whether those with chromosomal sex determination (CSD), the most common system, will better resist the influence of high temperature than those with polygenic sex determination (PSD). Here, we compared the effects of elevated temperature in two wild zebrafish strains, Nadia (NA) and Ekkwill (EKW), which have CSD with a ZZ/ZW system, against the AB laboratory strain, which has PSD. First, we uncovered novel sex genotypes and the results showed that, at control temperature, the masculinization rate roughly doubled with the addition of each Z chromosome, while some ZW and WW fish of the wild strains became neomales. Surprisingly, we found that at elevated temperatures WW fish were just as likely as ZW fish to become neomales and that all strains were equally susceptible to masculinization. These results demonstrate that the Z chromosome is not essential for male development and that the dose of W buffers masculinization at the control temperature but not at elevated temperature. Furthermore, at the elevated temperature the testes of neomales, but not of normal males, contained more spermatozoa than at the control temperature. Our results show in an unprecedented way that, in a global warming scenario, CSD species may not necessarily be better protected against the masculinizing effect of elevated temperature than PSD species, and reveal genotype-by-temperature interactions in male sex determination and spermatogenesis.
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spelling Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determinationGlobal warmingNeomalesSex determinationSex ratiosSex-reversalZebrafishSex ratio depends on sex determination mechanisms and is a key demographic parameter determining population viability and resilience to natural and anthropogenic stressors. There is increasing evidence that the environment can alter sex ratio even in genetically sex-determined species (GSD), as elevated temperature can cause female-to-male sex reversal (neomales). Alarmingly, neomales are being discovered in natural populations of several fish, amphibian and reptile species worldwide. Understanding the basis of neomale development is important for conservation biology. Among GSD species, it is unknown whether those with chromosomal sex determination (CSD), the most common system, will better resist the influence of high temperature than those with polygenic sex determination (PSD). Here, we compared the effects of elevated temperature in two wild zebrafish strains, Nadia (NA) and Ekkwill (EKW), which have CSD with a ZZ/ZW system, against the AB laboratory strain, which has PSD. First, we uncovered novel sex genotypes and the results showed that, at control temperature, the masculinization rate roughly doubled with the addition of each Z chromosome, while some ZW and WW fish of the wild strains became neomales. Surprisingly, we found that at elevated temperatures WW fish were just as likely as ZW fish to become neomales and that all strains were equally susceptible to masculinization. These results demonstrate that the Z chromosome is not essential for male development and that the dose of W buffers masculinization at the control temperature but not at elevated temperature. Furthermore, at the elevated temperature the testes of neomales, but not of normal males, contained more spermatozoa than at the control temperature. Our results show in an unprecedented way that, in a global warming scenario, CSD species may not necessarily be better protected against the masculinizing effect of elevated temperature than PSD species, and reveal genotype-by-temperature interactions in male sex determination and spermatogenesis.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)National Institutes of HealthMinisterio de Ciencia e InnovaciónInstitut de Ciències del Mar Consejo Superior de Investigaciones CientíficasInstitute of Neuroscience University of OregonReproductive and Molecular Biology Group Department of Structural and Functional Biology Institute of Biosciences São Paulo State UniversityReproductive and Molecular Biology Group Department of Structural and Functional Biology Institute of Biosciences São Paulo State UniversityFAPESP: 17/15793–7National Institutes of Health: 5R35 GM139635Ministerio de Ciencia e Innovación: AGL2016–787107-RFAPESP: FAPESP 14/07620–7National Institutes of Health: R01 GM085318Consejo Superior de Investigaciones CientíficasUniversity of OregonUniversidade Estadual Paulista (UNESP)Valdivieso, AlejandroWilson, Catherine A.Amores, Angelda Silva Rodrigues, Maira [UNESP]Nóbrega, Rafael Henrique [UNESP]Ribas, LaiaPostlethwait, John H.Piferrer, Francesc2023-03-02T06:28:14Z2023-03-02T06:28:14Z2022-10-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1016/j.envres.2022.113549Environmental Research, v. 213.1096-09530013-9351http://hdl.handle.net/11449/24197110.1016/j.envres.2022.1135492-s2.0-85132739703Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengEnvironmental Researchinfo:eu-repo/semantics/openAccess2023-03-02T06:28:14Zoai:repositorio.unesp.br:11449/241971Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462023-03-02T06:28:14Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
title Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
spellingShingle Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
Valdivieso, Alejandro
Global warming
Neomales
Sex determination
Sex ratios
Sex-reversal
Zebrafish
title_short Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
title_full Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
title_fullStr Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
title_full_unstemmed Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
title_sort Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
author Valdivieso, Alejandro
author_facet Valdivieso, Alejandro
Wilson, Catherine A.
Amores, Angel
da Silva Rodrigues, Maira [UNESP]
Nóbrega, Rafael Henrique [UNESP]
Ribas, Laia
Postlethwait, John H.
Piferrer, Francesc
author_role author
author2 Wilson, Catherine A.
Amores, Angel
da Silva Rodrigues, Maira [UNESP]
Nóbrega, Rafael Henrique [UNESP]
Ribas, Laia
Postlethwait, John H.
Piferrer, Francesc
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Consejo Superior de Investigaciones Científicas
University of Oregon
Universidade Estadual Paulista (UNESP)
dc.contributor.author.fl_str_mv Valdivieso, Alejandro
Wilson, Catherine A.
Amores, Angel
da Silva Rodrigues, Maira [UNESP]
Nóbrega, Rafael Henrique [UNESP]
Ribas, Laia
Postlethwait, John H.
Piferrer, Francesc
dc.subject.por.fl_str_mv Global warming
Neomales
Sex determination
Sex ratios
Sex-reversal
Zebrafish
topic Global warming
Neomales
Sex determination
Sex ratios
Sex-reversal
Zebrafish
description Sex ratio depends on sex determination mechanisms and is a key demographic parameter determining population viability and resilience to natural and anthropogenic stressors. There is increasing evidence that the environment can alter sex ratio even in genetically sex-determined species (GSD), as elevated temperature can cause female-to-male sex reversal (neomales). Alarmingly, neomales are being discovered in natural populations of several fish, amphibian and reptile species worldwide. Understanding the basis of neomale development is important for conservation biology. Among GSD species, it is unknown whether those with chromosomal sex determination (CSD), the most common system, will better resist the influence of high temperature than those with polygenic sex determination (PSD). Here, we compared the effects of elevated temperature in two wild zebrafish strains, Nadia (NA) and Ekkwill (EKW), which have CSD with a ZZ/ZW system, against the AB laboratory strain, which has PSD. First, we uncovered novel sex genotypes and the results showed that, at control temperature, the masculinization rate roughly doubled with the addition of each Z chromosome, while some ZW and WW fish of the wild strains became neomales. Surprisingly, we found that at elevated temperatures WW fish were just as likely as ZW fish to become neomales and that all strains were equally susceptible to masculinization. These results demonstrate that the Z chromosome is not essential for male development and that the dose of W buffers masculinization at the control temperature but not at elevated temperature. Furthermore, at the elevated temperature the testes of neomales, but not of normal males, contained more spermatozoa than at the control temperature. Our results show in an unprecedented way that, in a global warming scenario, CSD species may not necessarily be better protected against the masculinizing effect of elevated temperature than PSD species, and reveal genotype-by-temperature interactions in male sex determination and spermatogenesis.
publishDate 2022
dc.date.none.fl_str_mv 2022-10-01
2023-03-02T06:28:14Z
2023-03-02T06:28:14Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1016/j.envres.2022.113549
Environmental Research, v. 213.
1096-0953
0013-9351
http://hdl.handle.net/11449/241971
10.1016/j.envres.2022.113549
2-s2.0-85132739703
url http://dx.doi.org/10.1016/j.envres.2022.113549
http://hdl.handle.net/11449/241971
identifier_str_mv Environmental Research, v. 213.
1096-0953
0013-9351
10.1016/j.envres.2022.113549
2-s2.0-85132739703
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Environmental Research
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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