Evolution of an insect immune barrier through horizontal gene transfer mediated by a parasitic wasp

Genome sequencing data have recently demonstrated that eukaryote evolution has been remarkably influenced by the acquisition of a large number of genes by horizontal gene transfer (HGT) across different kingdoms. However, in depth-studies on the physiological traits conferred by these accidental DNA acquisitions are largely lacking. Here we elucidate the functional role of Sl gasmin, a gene of a symbiotic virus of a parasitic wasp that has been transferred to an ancestor of the moth species Spodoptera littoralis and domesticated. This gene is highly expressed in circulating immune cells (haemocytes) of larval stages, where its transcription is rapidly boosted by injection of microorganisms into the body cavity. RNAi silencing of Sl gasmin generates a phenotype characterized by a precocious suppression of phagocytic activity by haemocytes, which is rescued when these immune cells are incubated in plasma samples of control larvae, containing high levels of the encoded protein. Proteomic analysis demonstrates that the protein Sl gasmin is released by haemocytes into the haemolymph, where it opsonizes the invading bacteria to promote their phagocytosis, both in vitro and in vivo. Our results show that important physiological traits do not necessarily originate from evolution of pre-existing genes, but can be acquired by HGT events, through unique pathways of symbiotic evolution. These findings indicate that insects can paradoxically acquire selective advantages with the help of their natural enemies. Author summary Parasitic wasps are important insect biocontrol agents. These insects are beneficial for the ecological service they provide, which largely contributes to the control of natural populations of their hosts. Paradoxically, they can be beneficial also for non-host individuals attacked by mistake, if these survive after parasitization. In nature, this can happen to lepidopteran larvae when attacked by a wasp harbouring a symbiotic virus that can mediate horizontal gene transfer. Indeed, this virus, injected along with the egg in the body of the host, can get integrated in the genome of the parasitized larva, carrying along exogenous genes. Because the non-host regularly suppresses the parasitoid egg and/or juveniles, any surviving individual with a stable insertion of new genes in the germ line will represent an evolutionary novelty, with expanded functional capacities, if the resulting gene domestication event confers new physiological traits. The immune function here discovered demonstrates that symbiotic associations can drive unique evolutionary pathways, maximizing the fitness of interacting organisms, which evolve as a complex unit with a shared gene pool.