This demonstrates that this sequence might be a strain-specific sex marker in common carp. And we found no similarity between it and male-specific marker in bighead carp. Unlike the big carp, the sex-determination of zebrafish has been found to be both genetic and environmental. Chromosome 4 are closely-related to its sex, 58 but we found the male-specific region in bighead carp cannot mapped to that region in zebrafish genome.
Evolution of sex determination in fish
As to the common carp, which is a tetraploid fish, it might have formed its own sex-determination region or genes in its speciation process. Sex-specific markers have been successfully used to identify the sex determination systems in many species, 18 , 24 , 35—38 and it is especially valuable in species that lack heteromorphic sex chromosomes. Besides, the female-to-male segregation ratio in three full-sib families was 1 : 1.
And this system might persist in all extent species in Cyprinidae and facilitate the hybrid between different species within this group. Bighead carp and silver carp are two of the most closely related species of the Cyprinidae family, cytogenetic analyses revealed that they have similar karyotypes and lack visually heteromorphic sex chromosomes. In this study, bighead carp, silver carp and grass carp shared the same sex-specific markers and sex-determining DNA sequence, suggesting that they may have a homologous nascent Y chromosome and the same pathways involved in sex determination systems.
Therefore, the three carp should share the most recent common ancestor and the sex determination systems probably arose before speciation. We presented an approach that identifies and validates sex-specific markers using 2b-RAD sequencing and genome re-sequencing from multiple male and female individuals in bighead carp and silver carp.
A male-specific scaffold was identified and three sex-specific primers were designed first according the male-specific scaffold. In addition, all gynogenetic progenies were genetically sexed as female by these sex-specific markers, confirming the female homogamety sex determination system in bighead carp. The sex-specific markers developed in this study would be powerful and effective tools to uncover the sex determination system and identify potential genomic regions in bighead carp and silver carp. We would like to thank Xinhua Wang, Baojiang Gan and Xueli Liu for sample collection and laboratory technical assistance.
We would like to thank Prof. Shunping He for offering the bighead carp genome sequences. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account.
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Meixia Pang. Xiaomu Yu. Ying Zhou. Jingou Tong. Beide Fu. To whom correspondence should be addressed. Email: fubeide ihb. Edited by Dr Toshihiko Shiroishi. Cite Citation. Permissions Icon Permissions. Abstract Sex-specific markers are powerful tools for identifying sex-determination system in various animals. Table 2. Figure 1. Open in new tab Download slide. Figure 2. Figure 3. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Search ADS. Diversity and plasticity of sex determination and differentiation in fishes.
Evolutionary diversity and turn-over of sex determination in teleost fishes. Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture. Isolation of Y- and X-linked SCAR markers in yellow catfish and application in the production of all-male populations.
An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes Fugu. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle.
A tandem duplicate of anti-mullerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile tilapia , Oreochromis niloticus. Molecular basis and genetic improvement of economically important traits in aquaculture animals. Google Preview. The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals.
A sex-associated sequence identified by RAPD screening in gynogenetic individuals of turbot Scophthalmus maximus. AFLP analysis confirms exclusive maternal genomic contribution of meiogynogenetic sea bass Dicentrarchus labrax L. An AFLP-based approach for the identification of sex-linked markers in rainbow trout Oncorhynchus mykiss. Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish.
Identification of sex-specific markers reveals male heterogametic sex determination in Pseudobagrus ussuriensis. A transcriptome derived female-specific marker from the invasive western mosquitofish Gambusia affinis. Transcriptomic analyses reveal novel genes with sexually dimorphic expression in yellow catfish Pelteobagrus fulvidraco brain.
Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination. Characterization of gonadal transcriptomes from Nile tilapia Oreochromis niloticus reveals differentially expressed genes. A new SNP-based vision of the genetics of sex determination in European sea bass Dicentrarchus labrax.
Mapping the sex determination locus in the Atlantic halibut Hippoglossus hippoglossus using RAD sequencing. Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. Mapping and validation of the major sex-determining region in Nile tilapia Oreochromis niloticus L. Identification of sex-specific molecular markers using restriction site-associated DNA sequencing. Genomic characterization of sex-identification markers in Sebastes carnatus and S.
The draft genome of the grass carp Ctenopharyngodon idellus provides insights into its evolution and vegetarian adaptation. First report of Y-linked genes in the kissing bug Rhodnius prolixus. Centromere localization for bighead carp Aristichthys nobilis through half-tetrad analysis in diploid gynogenetic families. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Genomic approaches to study genetic and environmental influences on fish sex determination and differentiation.
Restriction site-associated DNA sequencing RAD-seq reveals an extraordinary number of transitions among gecko sex-determining systems. A novel male-specific DNA sequence in the common carp, Cyprinus carpio. The zebrafish reference genome sequence and its relationship to the human genome. Phylogenomic analysis resolves the formerly intractable adaptive diversification of the endemic clade of east Asian Cyprinidae Cypriniformes.
Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Comparative mapping for bighead carp Aristichthys nobilis against model and non-model fishes provides insights into the genomic evolution of cyprinids. For commercial re-use, please contact journals. Issue Section:. Download all figures.
Supplementary data. Supplementary Data. View Metrics. Email alerts New issue alert. Advance article alerts. The alignment of these sequences and highly related ones retrieved from GenBank Table 2 revealed the existence of variable sites and of parsimony informative sites.
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Phylogenetic analysis based on ML and BI phylogenetic tree reconstruction Figure 2 showed a topology with three main supported clades integrated by: 1 autosomic Dmrt1 sequences from O. Tetraodon nigroviridis Dmrt3 and Dmrt4 resulted in most divergent sequences of this data set which collapsed in a basal polytomy with the aforementioned clades. Later on juveniles and adults stages , the fragment was only detected in male individuals Figure 3. The corresponding translated fragment sequence included one stop codon.
The mRNA Dmrt1 sequence from Mus musculus is the most divergent and not well supported basal taxon which collapsed in a basal polytomy with the remaining aforementioned clades. This pattern was similar to O. It is worthy of notice that the same pattern was also found in the A. Thus, the smaller fragment is present in both sexes of the A.
In fish, five classes of Dmrt genes have been described: Dmrt 1 , 2 , 3 , 4 and 5 Huang et al. A moderate similarity was detected among the A. Therefore these results suggest a non conclusive relationship between the isolated fragments and the Dmrt1 from different fish groups.
Discover the progressive evolution of sex chromosomes
Another possibility could be that the DM domain is not present in the A. Phylogenetic relationships among DM domain containing genes are not obvious in vertebrates, as different taxa show little sequence conservation outside this domain Volff et al. Phylogenetic analyses grouped the A. This discordance may be explained by ancestral polymorphism maintenance or homoplasy. Evolution of homoplastic characters results from adaptations of different lineages in response to selective pressures in similar environments Futuyma, ; Wake et al.
Atheriniformes, Beloniformes and Cyprinodontiformes belong to the monophyletic Atherinomorpha Series. Beloniformes and Cyprinodontiformes are considered sister groups, while Atheriniformes occupies a basal position Parenti, ; Nelson, ; Setiamarga et al. Thus, this discordance may be explained by ancestral polymorphism maintenance, as in the topology the A. Furthermore, this clade is basally related with Odontesthes Atheriniformes Dmrt1 sequences. Discordance between Dmrt1 sequence relationships was also evidenced in phylogenetic analyses performed with Dmrt1 from O.
Although homology relationships among members of the Dmrt family have not been clearly established in metazoans, it is interesting to consider that the Dmrt1 gene is the closest related member in terms of structure and function to Drosophila dsx and Caenorhadbitis elegans mab-3 Herpin and Schartl, In this sense, all phylogenetic analyses in the present work straightforward grouped Drosophila dsx with A. The expression pattern of cDNA partial sequence during the ontogeny of the studied species showed that this sequence is detected from dispersed phase late blastula.
This suggests that its expression depends on the zygotic genome activation mid-blastula transition. In 1 to cell embryos this probability is, however, only 0.
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The probability of simultaneous occurrence of two or more independent events is calculated as the product of probabilities of each independent event Canavos, We assumed the probability for a given embryo to be male or female to be 0. For this reason, we consider that the absence of fragment amplification in these developmental stages indicates that it is not maternally supplied and that its expression depends on zygotic genome activation.
Oryzias latipes Dmrt1bY begins its expression during the neurula stage 1 day post fertilization , while Dmrt1a starts its expression during testis differentiation about 20 days post hatching Iwamatsu, ; Nanda et al. This observation is in contrast to data documented from different vertebrate species. For instance, Dmrt1 gene expression is identified later in ontogeny when a gonadal primordium is present mouse, Raymond et al. In most fish species analyzed, Dmrt1 gene expression was reported in post hatching stages C. However, these embryos are in somitogenesis Schulz et al.
Therefore, the finding that this cDNA partial sequence is expressed very early during A. Taken together, these results suggest that both isolated A. The observed male-specific expression pattern supports the hypothesis that this sequence probably belongs to an alternative splicing Dmrt1 gene version in A. Nevertheless, it is also possible that the isolated cDNA sequence belongs to a class of abundant non-coding RNAs with potential regulatory function. It has furthermore been documented that splicing isoforms encode a protein, whereas other specific splicing isoforms encode regulatory lncRNAs that show tissue specificity and dynamic expression during development Amaral et al.
The results obtained with RNAfold analysis Gruber et al. Nevertheless, it is essential to obtain more sequence information e. To further evaluate if this RNA is effectively translated characterization of expression pattern in temporal and spatial scales the generation of specific antibodies would be necessary. For sex determination studies in a given species it is important to consider the criterion proposed by Valenzuela et al. Sex chromosomes were, however, not identified in A.
Cytogenetically differentiated sex chromosomes are sporadic in different fish taxa, suggesting a recent and polyphyletic origin of sex chromosomes in this vertebrate group Mank et al. Fish sex chromosomes are difficult to evidence by classic cytogenetic techniques due to their putative recent origin homomorphic chromosomes. Ultrastructural analyses of synaptonemic complexes could reveal tiny unpaired regions allowing sex chromosome pair recognition in the heterogametic sex Devlin and Nagahama, This approach made it possible to identify sex chromosomes in O.
For this reason we cannot discard the presence of homomorphic sex chromosomes in A. Even in the absence of sex chromosomes, GSD may be demonstrated by the construction of a microsatellite-based linkage map to define genome regions involved in sex determination. This approach allowed the identification of the male sex determining non-recombinant region in the African annual fish Nothobranchius furzeri Valenzano et al.
We are very grateful for suggestions and improvements made by reviewers of this manuscript. Akaike H A new look at the statistical model identification. J Mol Biol Mamm Genome Nucleic Acids Res DD J Fish Biol Tissue Cell Eur J Neurosci McGraw Hill, Mexico, pp. Aquaculture Science Devlin RH and Nagahama Y Sex determination and sex differentiation in fish: An overview of genetic, physiological and environmental influences.
BMC Evol Biol 7:e Fish Physiol Biochem Sex Dev Futuyma DJ Evolution. Sinauer Associates, Sunderland, pp. J Zool Syst Evol Res Biol J Linn Soc Graves JA and Peichel C Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol Nucleic Acids Res WW Syst Biol J Mol Evol Cytogenet Genome Res BMC Dev Biol 7:e3. Plos Genetics 6:e Herpin A and Schartl M Dmrt1 genes at the crossroads: A widespread and central class of sexual development factors in fish.
FEBS J Hodgkin J The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: Ancestry or aptitude? Genes Dev J Exp Zool Biol Reprod Iwamatsu T Stages of normal development in the medaka Oryzias latipes. Zool Sci Gene The fish-specific Dmrt2b diverged from Dmrt2a before the fish whole-genome duplication. Genesis Kikuchi K and Hamaguchi S Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn Kimura M Estimation of evolutionary distances between homologous nucleotide sequences.
Kopp A Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet Reprod Biol Endocrinol Algorithms Mol Biol 6:e Biochem Biophys Res Commun Biochim Biophys Acta Nature BioTechniques Myers GS Annual fishes. Aquarium J Nelson JS Fishes of the World. Wiley, Hoboken, pp. PLoS One 4:e