Abstract Domestication of transposable elements has been extensively documented in vertebrates, but few examples have been reported in non-model organisms, particularly crustaceans. Here, we present Imagin (Integrase-like gene in MAlacostracans derived from GINger1), a gene family derived from a Ginger1 DNA transposon domesticated in the common ancestor of malacostracan crustaceans over 400 million years ago. We discovered Imagin in the kuruma shrimp Penaeus japonicus as a single-copy, multi-exon gene residing within a conserved intron of the methylmalonyl-CoA mutase (MMUT) gene. Comprehensive phylogenetic and structural analyses demonstrate that while Imagin orthologs are under strong purifying selection and retain the conserved H2C2 zinc-finger domain and integrase core, they have ubiquitously lost the catalytic DDE triad essential for endonuclease activity. These structural features indicate that Imagin has undergone molecular exaptation, abandoning its ancestral mobility for a host function. Consistent with this loss of enzymatic capacity, PjImagin protein accumulates predominantly in the cytosol of oocytes during early development, rather than the nucleus. This localization pattern implies that the gene has been co-opted for a non-catalytic role, potentially involving nucleic acid binding, during female gonadal development in penaeid shrimp. Furthermore, transcriptome data revealed divergent expression profiles across lineages, where Imagin is enriched in the ovaries of penaeid shrimp but predominantly in the testes of other decapods, such as crabs and lobsters. Imagin thus represents a novel case of TE evolution, illustrating a complex history of ancient domestication followed by structural remodeling and regulatory subfunctionalization.
Hao et al. (Fri,) studied this question.