title: Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes.
abstract: Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.
authors.affiliation: Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), 08003 Barcelona, Spain.
authors.forename: Laia
authors.identifier: 0000-0001-5538-6236
authors.initials: L
authors.lastname: Ribas
authors.affiliation: Reproductive Genomics Group, Temasek Life Sciences Laboratory, 117604, Singapore.
authors.forename: Woei Chang
authors.identifier: 0000-0001-9354-1647
authors.initials: WC
authors.lastname: Liew
authors.affiliation: Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), 08003 Barcelona, Spain.
authors.forename: Noèlia
authors.identifier: 0000-0002-0319-3448
authors.initials: N
authors.lastname: Díaz
authors.affiliation: Reproductive Genomics Group, Temasek Life Sciences Laboratory, 117604, Singapore.
authors.forename: Rajini
authors.identifier: 0000-0002-6357-5392
authors.initials: R
authors.lastname: Sreenivasan
authors.affiliation: Reproductive Genomics Group, Temasek Life Sciences Laboratory, 117604, Singapore; laszlo@tll.org.sg piferrer@icm.csic.es.|Department of Animal Sciences and Animal Husbandry, Georgikon Faculty, University of Pannonia, Keszthely H-8360, Hungary.|Centre for Comparative Genomics, Murdoch University, Murdoch, WA 6150, Australia.
authors.forename: László
authors.identifier: 0000-0001-5435-5948
authors.initials: L
authors.lastname: Orbán
authors.affiliation: Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), 08003 Barcelona, Spain; laszlo@tll.org.sg piferrer@icm.csic.es.
authors.forename: Francesc
authors.identifier: 0000-0003-0903-4736
authors.initials: F
authors.lastname: Piferrer
mesh_terms: D000818:Animals; D005260:Female; D018507:Gene Expression Regulation, Developmental; D063990:Gene Ontology; D006066:Gonads / Q000196:embryology / Q000254:growth & development / Q000378:metabolism*; D006358:Hot Temperature; D008297:Male; D023421:Models, Animal; D012733:Sex Differentiation / Q000235:genetics*; D012744:Sex Ratio; D013696:Temperature; D013737:Testis / Q000196:embryology / Q000254:growth & development / Q000378:metabolism; D059467:Transcriptome; D015027:Zebrafish / Q000235:genetics*; D029961:Zebrafish Proteins / Q000235:genetics
chemical_list: D029961:Zebrafish Proteins
keywords: global warming; masculinization; polygenic sex determination; temperature; zebrafish