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Invertebrates do not possess adaptive immunity but have evolved a variety of unique repertoires of innate immune sensors. In this study, we explored the immune diversity and specificity of invertebrates based on the lophotrochozoan RLRs, a major component in antiviral immune recognition. By annotating RLRs in the genomes of 58 representative species across metazoan evolution, we explored the gene expansion of RLRs in Lophotrochozoa. Of note, the N-terminal domains of lophotrochozoan RLRs showed the most striking diversity which evolved independently by domain grafting. Exon–intron structures were revealed to be prevalent in the domain grafting of lophotrochozoan RLRs based on an analysis of sibling paralogs and orthologs. In more than half of the cases, the mechanism of ‘exonization/pseudoexonization’ led to the generation of non-canonical N-terminal domains. Transcriptomic studies revealed that many non-canonical RLRs display immune-related expression patterns. Two of these RLRs showed obvious evidence of positive selection, which may be the result of host defense selection pressure. Overall, our study suggests that the complex and unique domain arrangement of lophotrochozoan RLRs might result from domain grafting, exon–intron divergence, expression diversification, and positive selection, which may have led to functionally distinct lophotrochozoan RLRs.

Divergences of the RLR Gene Families across Lophotrochozoans: Domain Grafting, Exon–Intron Structure, Expression, and Positive Selection