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Animal taxa show remarkable variability in sexual reproduction, where separate sexes, or gonochorism, is thought to have evolved from hermaphroditism for most cases. Hermaphroditism accounts for 5% in animals, and sequential hermaphroditism has been found in teleost. In this study, we characterized a novel form of the transient hermaphroditic stage in little yellow croaker ( Larimichthys polyactis ) during early gonadal development. The ovary and testis were indistinguishable from 7 to 40 days post-hatching (dph). Morphological and histological examinations revealed an intersex stage of male gonads between 43 and 80 dph, which consist of germ cells, somatic cells, efferent duct, and early primary oocytes (EPOs). These EPOs in testis degenerate completely by 90 dph through apoptosis yet can be rescued by exogenous 17- β -estradiol. Male germ cells enter the mitotic flourishing stage before meiosis is initiated at 180 dph, and they undergo normal spermatogenesis to produce functional sperms. This transient hermaphroditic stage is male-specific, and the ovary development appears to be normal in females. This developmental pattern is not found in the sister species Larimichthys crocea or any other closely related species. Further examinations of serum hormone levels indicate that the absence of 11-ketotestosterone and elevated levels of 17- β -estradiol delineate the male intersex gonad stage, providing mechanistic insights on this unique phenomenon. Our research is the first report on male-specific transient hermaphroditism and will advance the current understanding of fish reproductive biology. This unique gonadal development pattern can serve as a useful model for studying the evolutionary relationship between hermaphroditism and gonochorism, as well as teleost sex determination and differentiation strategies.
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Dmrt1 is the only male pathway gene tested indispensable for sex determination and functional testis development in tilapia
Sex is determined by multiple factors derived from somatic and germ cells in vertebrates. We have identifiedamhy,dmrt1,gsdfas male andfoxl2,foxl3,cyp19a1aas female sex determination pathway genes in Nile tilapia. However, the relationship among these genes is largely unclear. Here, we found that the gonads ofdmrt1;cyp19a1adouble mutants developed as ovaries or underdeveloped testes with no germ cells irrespective of their genetic sex. In addition, the gonads ofdmrt1;cyp19a1a;cyp19a1btriple mutants still developed as ovaries. The gonads offoxl3;cyp19a1adouble mutants developed as testes, while the gonads ofdmrt1;cyp19a1a;foxl3triple mutants eventually developed as ovaries. In contrast, the gonads ofamhy;cyp19a1a,gsdf;cyp19a1a,amhy;foxl2,gsdf;foxl2double andamhy;cyp19a1a;cyp19a1b,gsdf;cyp19a1a;cyp19a1btriple mutants developed as testes with spermatogenesis via up-regulation ofdmrt1in both somatic and germ cells. The gonads ofamhy;foxl3andgsdf;foxl3double mutants developed as ovaries but with germ cells in spermatogenesis due to up-regulation ofdmrt1. Taking the respective ovary and underdeveloped testis ofdmrt1;foxl3anddmrt1;foxl2double mutants reported previously into consideration, we demonstrated that oncedmrt1mutated, the gonad could not be rescued to functional testis by mutating any female pathway gene. The sex reversal caused by mutation of male pathway genes other thandmrt1, including its upstreamamhyand downstreamgsdf, could be rescued by mutating female pathway gene. Overall, our data suggested thatdmrt1is the only male pathway gene tested indispensable for sex determination and functional testis development in tilapia.
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- Award ID(s):
- 1830753
- PAR ID:
- 10561667
- Editor(s):
- Schartl, Manfred
- Publisher / Repository:
- PLoS
- Date Published:
- Journal Name:
- PLOS Genetics
- Volume:
- 20
- Issue:
- 3
- ISSN:
- 1553-7404
- Page Range / eLocation ID:
- e1011210
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pgen.1011210
