Sex Determination and Differentiation in Fish

Guiguen, Yann; Fostier, Alexis; Herpin, Amaury

doi:10.1002/9781119127291.ch2

Cited by 20 publications

(13 citation statements)

References 156 publications

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“…These results not only strongly support the proposed origin via centric fusion between two non-homologous acrocentric chromosomes, but also that this event might have been fixed in P. semifasciata relatively recently, as WCP revealed preservation of all orthologous chromosomes in related Pyrrhulina species without apparent major divergence or rearrangements. As CGH results did not show clustering of sex-specific sequences on any chromosome of the P. brevis complement, it remains to be investigated, whether any of four PSEMI-Y labeled chromosomes represent cryptic (homomorphic) sex chromosomes with a sex-specific region being under resolution limit of the CGH method, or whether sex chromosomes are not present at all in this species and the sex determination is governed by other means (Herpin and Schartl, 2015; Guiguen et al, 2019).…”

Section: Discussionmentioning

confidence: 90%

“…Although the different 2n present in males (41) and females (42) could also indicate the occurrence of an X0 sex system, our CGH and particularly WCP results confirmed the occurrence of a multiple X 1 X 2 Y sex chromosome system in P. semifasciata . Though fishes possess an amazing variety of sex determination and differentiation mechanisms (Devlin and Nagahama, 2002; Herpin and Schartl, 2015; Schartl et al, 2016; Guiguen et al, 2019), sex chromosomes have been described only in about 5% of cytogenetically analyzed species (based on Arai, 2011). It is, however, increasingly apparent that this information is skewed by frequent presence of homomorphic (i.e., cytogenetically unrecognizable) fish gonosomes, which goes hand in hand with their relative evolutionary “youth” and predisposition to frequent sex chromosome turnovers in closely related species or even within species (Kitano and Peichel, 2012; Pennell et al, 2015; Gamble, 2016; Schartl et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

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Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

et al. 2019

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Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis . Our results showed 2n = 42 in both sexes of P. brevis , while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X 1 X 2 Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male- vs .-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species’ genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P . semifasciata -derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X 1 and X 2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general.

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Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

et al. 2019

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“…These genes include amhr2 , cyp11a , hsd3b2 , nr3c1 , sox9 , vasa , and gsdf ( Figure 3C ). Here, it is worth noting that allelic diversification of amhr2 in Takigugu rubripes results in a dominant master sex-determining gene, while allelic diversification of gsdf has given rise to the sex-determining gene in some fish species, including Oryzias luzonensis and Anoplopoma fimbria (reviewed in Piferrer, 2018; Guiguen et al, 2019). DNA methylation levels of amhr2 in the European sea bass were ∼50% without sex-related differences (Anastasiadi et al, 2018b), while in the half-smooth tongue sole DNA methylation levels are higher in females (Shao et al, 2014).…”

Section: Testing the Model Of The Conserved Epigenetic Regulation Of Sexmentioning

confidence: 99%

The Model of the Conserved Epigenetic Regulation of Sex

et al. 2019

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Epigenetics integrates genomic and environmental information to produce a given phenotype. Here, the model of Conserved Epigenetic Regulation of Sex (CERS) is discussed. This model is based on our knowledge on genes involved in sexual development and on epigenetic regulation of gene expression activation and silencing. This model was recently postulated to be applied to the sexual development of fish, and it states that epigenetic and gene expression patterns are more associated with the development of a particular gonadal phenotype, e.g., testis differentiation, rather than with the intrinsic or extrinsic causes that lead to the development of this phenotype. This requires the existence of genes with different epigenetic modifications, for example, changes in DNA methylation levels associated with the development of a particular sex. Focusing on DNA methylation, the identification of CpGs, the methylation of which is linked to sex, constitutes the basis for the identification of Essential Epigenetic Marks (EEM). EEMs are defined as the number and identity of informative epigenetic marks that are strictly necessary, albeit perhaps not sufficient, to bring about a specific, measurable, phenotype of interest. Here, we provide a summary of the genes where DNA methylation has been investigated so far, focusing on fish. We found that cyp19a1a and dmrt1, two key genes for ovary and testis development, respectively, consistently show an inverse relationship between their DNA methylation and expression levels, thus following CERS predictions. However, in foxl2a, a pro-female gene, and amh, a pro-male gene, such relationship is not clear. The available data of other genes related to sexual development such as sox9, gsdf, and amhr2 are also discussed. Next, we discuss the use of CERS to make testable predictions of how sex is epigenetically regulated and to better understand sexual development, as well as the use of EEMs as tools for the diagnosis and prognosis of sex. We argue that CERS can aid in focusing research on the epigenetic regulation of sexual development not only in fish but also in vertebrates in general, particularly in reptiles with temperature sex-determination, and can be the basis for possible practical applications including sex control in aquaculture and also in conservation biology.

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“…Teleost fish are the largest and most diverse group of vertebrates and provide many opportunities to study the evolution of sex determination (SD) systems. SD mechanisms of teleost fish can be divided into three types: genetic SD (GSD), environmental SD (ESD), and a combination of GSD and ESD [1]. In GSD systems, master sex-determining (MSD) genes are thought to play a crucial role in gonad differentiation by regulating the expression of other genes.…”

Section: Introductionmentioning

confidence: 99%

A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific

et al. 2021

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Teleost fish are the most diverse group of vertebrates and provide opportunities to study the evolution of sex determination (SD) systems. Using genomic and functional analyses, we identified a male-specific duplication of anti-Müllerian hormone ( amh ) gene as the male master sex-determining (MSD) gene in Sebastes schlegelii . By resequencing 10 males and 10 females, we characterized a 5 kb-long fragment in HiC_Scaffold_12 as a male-specific region, which contained an amh gene (named amhy ). We then demonstrated that amhy is a duplication of autosomal amh that was later translocated to the ancestral Y chromosome. amha and amhy shared high-nucleotide identity with the most significant difference being two insertions in intron 4 of amhy . Furthermore, amhy overexpression triggered female-to-male sex reversal in S. schlegelii , displaying its fundamental role in driving testis differentiation. We developed a PCR assay which successfully identified sexes in two species of northwest Pacific rockfish related to S. schlegelii . However, the PCR assay failed to distinguish the sexes in a separate clade of northeast Pacific rockfish. Our study provides new examples of amh as the MSD in fish and sheds light on the convergent evolution of amh duplication as the driving force of sex determination in different fish taxa.

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Sex Determination and Differentiation in Fish

Cited by 20 publications

References 156 publications

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

The Model of the Conserved Epigenetic Regulation of Sex

A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific

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