Transposon insertion into pmel-17 reduced melanin pigmentation, and growth, but increased locomotion of Mozambique tilapia

One fundamental goal in biology is to understand genotype–environment–phenotype relationships. Transposable elements play important roles in phenotypic variations, particularly in species with recent expansions of these elements, by acting on their flanking genes via different mechanisms. Previous studies showed that in Mozambique tilapia, pmel-17 determines the golden and black color, and the insertion of a 133–148 bp fragment in the 3’ UTR of this gene was the causal variant for the golden colors. However, how this gene determines skin color remains elusive. Here, using long-read sequencing technology, we found that a ∼ 3.7 kb African cichlid-specific transposon, DRMTP (DNA repeat from the Mozambique tilapia pmel locus), was inserted into the 3’ UTR of pmel-17 of Mozambique tilapia. This insertion led to loss of melanin pigmentation, reduced growth performance, and increased locomotion. Methylation and reporter gene assays show that DRMTP suppresses pmel-17 expression by both epigenetic silencing and DNA secondary structure induced by the transposon per se. Our data provide novel insights into how a single gene is regulated by a transposon and affects multiple phenotypes. A single gene can determine multiple phenotypes, among which some might not be preferred for aquaculture. Therefore, the overall effects of the changes in a single or a few major-effect genes for a trait, on other economic traits and environment, should be evaluated before they are used in selective breeding programs.