Redistribution of ancestral functions underlies the evolution of venom production in marine predatory snails

Venom-secreting glands are highly specialised organs evolved throughout the animal kingdom to synthetise and secrete toxins for predation and defence. Venom is extensively studied for its toxin components and application potential; yet, how animals become venomous remains poorly understood. Venom systems therefore offer a unique opportunity to understand the molecular mechanisms underlying functional innovation. Here, we conducted a multi-species multi-tissue comparative transcriptomics analysis of 12 marine predatory gastropod species, including species with venom glands and species with homologous non-venom producing glands, to examine how specialised functions evolve through gene expression changes. We found that while the venom gland specialised for the mass production of toxins, its homologous glands retained the ancestral digestive functions. The functional divergence and specialisation of the venom gland was achieved through a redistribution of its ancestral digestive functions to other organs, specifically the oesophagus. This entailed concerted expression changes and accelerated transcriptome evolution across the entire digestive system. The increase in venom gland secretory capacity was achieved through the modulation of an ancient secretory machinery, particularly genes involved in endoplasmic reticulum stress and unfolded protein response. This study shifts the focus from the well-explored evolution of toxins to the lesser-known evolution of the organ and mechanisms responsible for venom production. As such, it contributes to elucidating the molecular mechanisms underlying organ evolution at a fine evolutionary scale, highlighting the specific events that lead to functional divergence.