Environmentally-induced sex reversal in fish with chromosomal vs. polygenic sex determination
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , |
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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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:29462024-08-05T19:39:50.097565Repositório 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) |
repository.mail.fl_str_mv |
|
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1808129103896772608 |