Early fish domestication affects methylation of key genes involved in the rapid onset of the farmed phenotype

ABSTRACT

Animal domestication is a process of environmental modulation and artificial selection leading to permanent phenotypic modifications. Recent studies showed that phenotypic changes occur very early in domestication, i.e., within the first generation in captivity, which raises the hypothesis that epigenetic mechanisms may play a critical role on the early onset of the domestic phenotype. In this context, we applied reduced representation bisulphite sequencing to compare methylation profiles between wild Nile tilapia females and their offspring reared under farmed conditions. Approximately 700 differentially methylated CpG sites were found, many of them associated not only with genes involved in muscle growth, immunity, autophagy and diet response but also related to epigenetic mechanisms, such as RNA methylation and histone modifications. This bottom-up approach showed that the phenotypic traits often related to domestic animals (e.g., higher growth rate and different immune status) may be regulated epigenetically and prior to artificial selection on gene sequences. Moreover, it revealed the importance of diet in this process, as reflected by differential methylation patterns in genes critical to fat metabolism. Finally, our study highlighted that the TGF-β1 signalling pathway may regulate and be regulated by several differentially methylated CpG-associated genes. This could be an important and multifunctional component in promoting adaptation of fish to a domestic environment while modulating growth and immunity-related traits.

KEYWORDS:

• Domestication
• epigenetics
• DNA methylation
• muscle growth
• Oreochromis niloticus

Acknowledgments

We are thankful to Hilde Ribe, Øivind Torslett, Steinar Johnsen and Kaspar Klaudiussen (Nord University, Norway) for their assistance in fish husbandry and commitment to the welfare of the fish. This study has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no 683210) and from the Research Council of Norway under the Toppforsk programme(grant agreement no 250548/F20).

Disclosure statement

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

Additional information

Funding

This work was supported by the H2020 European Research Council [683210]; Norges Forskningsråd [250548/F20].