DNA hydroxymethylation differences underlie phenotypic divergence of somatic growth in Nile tilapia reared in common garden

ABSTRACT

Phenotypic plasticity of metabolism and growth are essential for adaptation to new environmental conditions, such as those experienced during domestication. Epigenetic regulation plays a key role in this process but the underlying mechanisms are poorly understood, especially in the case of hydroxymethylation. Using reduced representation 5-hydroxymethylcytosine profiling, we compared the liver hydroxymethylomes in full-sib Nile tilapia with distinct growth rates (3.8-fold difference) and demonstrated that DNA hydroxymethylation is strongly associated with phenotypic divergence of somatic growth during the early stages of domestication. The 2677 differentially hydroxymethylated cytosines between fast- and slow-growing fish were enriched within gene bodies (79%), indicating a pertinent role in transcriptional regulation. Moreover, they were found in genes involved in biological processes related to skeletal system and muscle structure development, and there was a positive association between somatic growth and 5hmC levels in genes coding for growth factors, kinases and receptors linked to myogenesis. Single nucleotide polymorphism analysis revealed no genetic differentiation between fast- and slow-growing fish. In addition to unveiling a new link between DNA hydroxymethylation and epigenetic regulation of growth in fish during the initial stages of domestication, this study suggests that epimarkers may be applied in selective breeding programmes for superior phenotypes.

GRAPHICAL ABSTRACT

KEYWORDS:

• Epigenetics
• DNA hydroxymethylation
• domestication
• somatic growth
• teleosts
• phenotypic plasticity

Acknowledgments

We are thankful to Mr Kaspar Klaudiussen (Nord University) for the outstanding care of our Nile tilapia and assistance with sampling.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Ethics approval

All procedures involving animals were in accordance with the EU Directive 2010/63 on the use of animals for scientific purposes and were approved by Nord University’s ethics committee and the Norwegian Animal Research Authority (FOTS licence no. 1042).

Data availability statement

The DNA hydroxymethylation dataset generated in this study has been submitted to the NCBI Sequence Read Archive (SRA) repository, under the accession number PRJNA665120.

Author contributions

IK carried out the sampling, generated the RRHP libraries, performed the bioinformatic analysis, interpreted the results and wrote the research article. PS contributed to the bioinformatic analysis and interpretation of the RRHP dataset, and revised the article. MSOB and KSJ contributed to the bioinformatic analysis and discovery of single nucleotide polymorphisms using the RRHP dataset, and they revised the article. HL, CP, and TT carried out the sampling, wet lab and revised the article. JMOF conceived the study, provided reagents and consumables, contributed to the interpretation of the results and revised the manuscript.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15592294.2023.2282323

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.

Additional information

Funding

This work was funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no 683210 to JMOF) and by Research Council of Norway under the Toppforsk programme (grant agreement no 250548/F20 to JMOF).