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DdRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23.

ABSTRACT: In Nile tilapia sex determination is governed by a male heterogametic system XX/XY either on LG1 or LG23. The latter carries a Y-specific duplicate of the amh gene, which is a testis-determining factor. Allelic variants in the amh gene demonstrated to be major triggers for autosomal and temperature-dependent sex reversal. Further, QTL on LG23 and LG20 show a temperature-responsiveness with influence on the phenotypic sex relative to the sex chromosomes. Here we present a ddRADseq based approach to identify genomic regions that show unusual large differentiation in terms of fixation index (FST) between temperature-treated pseudomales and non-masculinized females using a comparative genome-scan. Genome-wide associations were identified for the temperature-dependent sex using a genetically all-female population devoid of amh-?Y.Twenty-two thousand three hundred ninety-two SNPs were interrogated for the comparison of temperature-treated pseudomales and females, which revealed the largest differentiation on LG23. Outlier FST-values (0.35-0.44) were determined for six SNPs in the genomic interval (9,190,077-11,065,693) harbouring the amh gene (9,602,693-9,605,808), exceeding the genome-wide low FST of 0.013. Association analysis with a set of 9104 selected SNPs confirmed that the same genomic region on LG23 exerts a significant effect on the temperature-dependent sex.This study highlights the role of LG23 in sex determination, harbouring major determinants for temperature-dependent sex reversal in Nile tilapia. Furthermore FST outlier detection proves a powerful tool for detection of sex-determining regions in fish genomes.

SUBMITTER: Wessels S

PROVIDER: S-EPMC5513378 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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ddRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23.

Wessels Stephan S Krause Ina I Floren Claudia C Schütz Ekkehard E Beck Jule J Knorr Christoph C

BMC genomics 20170714 1

<h4>Background</h4>In Nile tilapia sex determination is governed by a male heterogametic system XX/XY either on LG1 or LG23. The latter carries a Y-specific duplicate of the amh gene, which is a testis-determining factor. Allelic variants in the amh gene demonstrated to be major triggers for autosomal and temperature-dependent sex reversal. Further, QTL on LG23 and LG20 show a temperature-responsiveness with influence on the phenotypic sex relative to the sex chromosomes. Here we present a ddRAD ...[more]

PMID: 28705237

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Project description:Nile tilapia (Oreochromis niloticus) is an African freshwater fish that displays a genetic sex determination system (XX|XY) where high temperatures (above 32°C to 36.5°C) induce masculinization. In Nile tilapia, the thermosensitive period was reported from 10 to 30 days post fertilization. In their natural environment, juveniles may encounter high temperatures that are above the optimal temperature for growth (27-30°C). The relevance of the thermal sex reversal mechanism in a natural context remains unclear. The main objective of our study is to determine whether sexually undifferentiated juveniles spontaneously prefer higher, unfavorable temperatures and whether this choice skews the sex ratio toward males. Five full-sib progenies (from 100% XX crosses) were subjected to (1) a horizontal three-compartment thermal step gradient (thermal continuum 28°C- 32°C- 36.5°C) during the thermosensitive period, (2) a control continuum (28°C- 28°C- 28°C) and (3) a thermal control tank (36.5°C). During the first days of the treatment, up to an average of 20% of the population preferred the masculinizing compartment of the thermal continuum (36.5°C) compared to the control continuum. During the second part of the treatment, juveniles preferred the lower, nonmasculinizing 32°C temperature. This short exposure to higher temperatures was sufficient to significantly skew the sex ratio toward males, compared to congeners raised at 28°C (from 5.0 ± 6.7% to 15.6 ± 16.5% of males). The proportion of males was significantly different in the thermal continuum, thermal control tank and control continuum, and it was positively correlated among populations. Our study shows for the first time that Nile tilapia juveniles can choose a masculinizing temperature during a short period of time. This preference is sufficient to induce sex reversal to males within a population. For the first time, behavior is reported as a potential player in the sex determination mechanism of this species.

Project description:Owing to the demand for sustainable sex-control protocols in aquaculture, research in tilapia sex determination is gaining momentum. The mutual influence of environmental and genetic factors hampers disentangling the complex sex determination mechanism in Nile tilapia (Oreochromis niloticus). Previous linkage analyses have demonstrated quantitative trait loci for the phenotypic sex on linkage groups 1, 3, and 23. Quantitative trait loci for temperature-dependent sex reversal similarly reside on linkage group 23. The anti-Müllerian hormone gene (amh), located in this genomic region, is important for sexual fate in higher vertebrates, and shows sexually dimorphic expression in Nile tilapia. Therefore this study aimed at detecting allelic variants and marker-sex associations in the amh gene. Sequencing identified six allelic variants. A significant effect on the phenotypic sex for SNP ss831884014 (p<0.0017) was found by stepwise logistic regression. The remaining variants were not significantly associated. Functional annotation of SNP ss831884014 revealed a non-synonymous amino acid substitution in the amh protein. Consequently, a fluorescence resonance energy transfer (FRET) based genotyping assay was developed and validated with a representative sample of fish. A logistic linear model confirmed a highly significant effect of the treatment and genotype on the phenotypic sex, but not for the interaction term (treatment: p<0.0001; genotype: p<0.0025). An additive genetic model proved a linear allele substitution effect of 12% in individuals from controls and groups treated at high temperature, respectively. Moreover, the effect of the genotype on the male proportion was significantly higher in groups treated at high temperature, giving 31% more males on average of the three genotypes. In addition, the groups treated at high temperature showed a positive dominance deviation (+11.4% males). In summary, marker-assisted selection for amh variant ss831884014 seems to be highly beneficial to increase the male proportion in Nile tilapia, especially when applying temperature-induced sex reversal.

Project description:BACKGROUND:Fish species often exhibit significant sexual dimorphism for commercially important traits. Accordingly, the control of phenotypic sex, and in particular the production of monosex cultures, is of particular interest to the aquaculture industry. Sex determination in the widely farmed Nile tilapia (Oreochromis niloticus) is complex, involving genomic regions on at least three chromosomes (chromosomes 1, 3 and 23) and interacting in certain cases with elevated early rearing temperature as well. Thus, sex ratios may vary substantially from 50%. RESULTS:This study focused on mapping sex-determining quantitative trait loci (QTL) in families with skewed sex ratios. These included four families that showed an excess of males (male ratio varied between 64% and 93%) when reared at standard temperature (28°C) and a fifth family in which an excess of males (96%) was observed when fry were reared at 36°C for ten days from first feeding. All the samples used in the current study were genotyped for two single-nucleotide polymorphisms (rs397507167 and rs397507165) located in the expected major sex-determining region in linkage group 1 (LG 1). The only misassigned individuals were phenotypic males with the expected female genotype, suggesting that those offspring had undergone sex-reversal with respect to the major sex-determining locus. We mapped SNPs identified from double digest Restriction-site Associated DNA (ddRAD) sequencing in these five families. Three genetic maps were constructed consisting of 641, 175 and 1,155 SNPs from the three largest families. QTL analyses provided evidence for a novel genome-wide significant QTL in LG 20. Evidence was also found for another sex-determining QTL in the fifth family, in the proximal region of LG 1. CONCLUSIONS:Overall, the results from this study suggest that these previously undetected QTLs are involved in sex determination in the Nile tilapia, causing sex reversal (masculinisation) with respect to the XX genotype at the major sex-determining locus in LG 1.

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DdRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23.

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ddRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23.

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