Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 114, Issue 6, Pages E941-E950Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1609411114
Keywords
zebrafish; temperature; masculinization; polygenic sex determination; global warming
Categories
Funding
- National Research Foundation, Prime Minister's Office, Singapore under its Competitive Research Programme [NRF-CRP7-2010-01]
- Agri-Food and Veterinary Authority of Singapore
- Temasek Life Sciences Laboratory
- Spanish Government Grants Aquagenomics [CDS2007-0002]
- Epigen-Aqua [AGL2010-15939]
- Epifarm [AGL2013-41047-R]
- Xarxa de Recerca d'Aquicultura (XRAq) grant
- Epigen-Aqua
- Epifarm
- CSIC [i-LINK0195]
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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.
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