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Hypoxia turns genotypic female medaka fish into phenotypic males

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Abstract

Hypoxia caused by eutrophication is amongst the most pressing global problems in aquatic systems. Notably, more than 400 “dead zones” have been identified worldwide, resulting in large scale collapse of fisheries and major changes in the structure and trophodynamics. Recent studies further discovered that hypoxia can also disrupt sex hormone metabolism and alter the sexual differentiation of fish, resulting in male biased F1 generations and therefore posing a threat to the sustainability of natural populations. However, it is not known whether, and if so how, hypoxia can also change the sex ratio in vertebrates that have sex-determining XX/XY chromosomes. Using the Japanese medaka (Oryzias latipes) as a model, we demonstrate, for the first time, that hypoxia can turn genotypic female fish with XX chromosomes into phenotypic males. Over half of the XX females exposed to hypoxia exhibit male secondary sexual characteristics and develop testis instead of ovary. We further revealed that hypoxia can: (a) down-regulate the vasa gene, which controls proliferation of primordial germ cells and gonadal sex differentiation into ovary, and (b) up-regulate the DMY gene which resides at the sex-determining locus of the Y chromosome, and direct testis differentiation. This is the first report that hypoxia can directly act on genes that regulate sex determination and differentiation, thereby turning genotypic females into phenotypic males and leading to a male-dominant F1 population.

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Acknowledgments

The work described in this paper was supported by a Grant from the University Grants Committee of the Hong Kong Special Administrative Region, China (AoE/P-04/04) and a postgraduate student granted to Catis Cheung by the City University of Hong Kong.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biology and Chemistry, City University of Hong Kong, Kowloon, Hong Kong, SAR, China

    Catis Hin Ying Cheung

  2. Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, SAR, China

    Jill Man Ying Chiu

  3. School of Biological Sciences, The University of Hong Kong, Pokfulam, Room 6N-01, Kadoorie Biological Sciences Building, Hong Kong, SAR, China

    Rudolf Shiu Sun Wu

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  1. Catis Hin Ying Cheung
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  2. Jill Man Ying Chiu
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Correspondence to Rudolf Shiu Sun Wu.

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Cheung, C.H.Y., Chiu, J.M.Y. & Wu, R.S.S. Hypoxia turns genotypic female medaka fish into phenotypic males. Ecotoxicology 23, 1260–1269 (2014). https://doi.org/10.1007/s10646-014-1269-8

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