Evolution of venom production in marine predatory snails

Abstract

Venom is a widespread secretion in nature, extensively studied for its toxin components and application potential. Yet, the evolution of venom production remains poorly understood. To address this question, we conducted a comparative transcriptomics analysis of the oesophagus-associated glands in marine predatory gastropods, among which the cone snail venom gland represents a pinnacle of specialisation. We found that 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. On the other hand, the emergence of novel genes, involving transposable elements, contributed to the gland regulatory network. Our analysis provides new insights into the genetic basis of functional divergence and highlights the remarkable plasticity of the gastropod digestive system.