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Differences in the fast muscle methylome provide insight into sex-specific epigenetic regulation of growth in Nile tilapia during early stages of domestication.

ABSTRACT: Growth is a complex trait whose variability within a population cannot be explained solely by genetic variation. Epigenetic regulation is often suggested as an important factor shaping the phenotype, but its association with growth can be highly context- and species-dependent. Nevertheless, the mechanisms involved in epigenetic regulation of growth in fish are poorly understood. We have used reduced representation bisulphite sequencing to determine the genome-wide CpG methylation patterns in male and female Nile tilapia of different sizes but at the same early stage of domestication. The average CpG methylation level in the reduced genome representation was 63% across groups but many sites displayed group-specific methylation patterns. The number of differentially methylated (DM) CpGs was much higher when the interaction between sex and weight was included rather than when these factors were considered separately. There were 1128 DM CpGs between large and small females and 970 DM CpGs between large and small males. We have found many growth-related genes associated with DM CpGs, namely map3k5 and akt3 in females and gadd45g and ppargc1a in males. Only 5% of CpG locations associated with growth were common to both sexes. In particular, the autophagy-related gene atg14 displayed a high association of methylation with growth exclusively in males. The sexually dimorphic association between atg14 methylation and growth may uncover novel metabolic mechanisms at play during mouth brooding in Nile tilapia females. Taken together, our data suggest that epigenetic regulation of growth in Nile tilapia involves different gene networks in males and females.

SUBMITTER: Podgorniak T

PROVIDER: S-EPMC6597363 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Differences in the fast muscle methylome provide insight into sex-specific epigenetic regulation of growth in Nile tilapia during early stages of domestication.

Podgorniak Tomasz T Brockmann Sven S Konstantinidis Ioannis I Fernandes Jorge M O JMO

Epigenetics 20190525 8

Growth is a complex trait whose variability within a population cannot be explained solely by genetic variation. Epigenetic regulation is often suggested as an important factor shaping the phenotype, but its association with growth can be highly context- and species-dependent. Nevertheless, the mechanisms involved in epigenetic regulation of growth in fish are poorly understood. We have used reduced representation bisulphite sequencing to determine the genome-wide CpG methylation patterns in mal ...[more]

PMID: 31131688

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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.

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:Nile tilapia (Oreochromis niloticus) is among the most farmed finfish worldwide, distributed across different environmental conditions. Its wide distribution has mainly been facilitated by several breeding programs and widespread dissemination of genetically improved strains. In the first Nile tilapia study exploiting a whole-genome pooled sequencing (Poolseq) approach, we identified the genetic structure and signatures of selection in diverse, farmed Nile tilapia populations, with a particular focus on the GIFT strain, developed in the 1980s, and currently managed by WorldFish (GIFTw). We also investigated important farmed strains from The Philippines and Africa. Using both SNP array data and Poolseq SNPs, we characterized the population structure of these samples. We observed the greatest separation between the Asian and African populations and greater admixture in the Asian populations than in the African ones. We also established that the SNP array data were able to successfully resolve relationships between these diverse Nile tilapia populations. The Poolseq data identified genomic regions with high levels of differentiation (F ST) between GIFTw and the other populations. Gene ontology terms associated with mesoderm development were significantly enriched in the genes located in these regions. A region on chromosome Oni06 was genetically differentiated in pairwise comparisons between GIFTw and all other populations. This region contains genes associated with muscle-related traits and overlaps with a previously published QTL for fillet yield, suggesting that these traits may have been direct targets for selection on GIFT. A nearby region was also identified using XP-EHH to detect genomic differentiation using the SNP array data. Genomic regions with high or extended homozygosity within each population were also identified. This study provides putative genomic landmarks associated with the recent domestication process in several Nile tilapia populations, which could help to inform their genetic management and improvement.

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Differences in the fast muscle methylome provide insight into sex-specific epigenetic regulation of growth in Nile tilapia during early stages of domestication.

Publications

Differences in the fast muscle methylome provide insight into sex-specific epigenetic regulation of growth in Nile tilapia during early stages of domestication.

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