Zancolli Giulia, Modica Maria Vittoria, Puillandre Nicolas, Kantor Yuri, Barua Agneesh, Campli Giulia, Robinson-Rechavi Marc
Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland.
Evolutionary Bioinformatics, Swiss Institute of Bioinformatics, Lausanne, Switzerland.
Mol Biol Evol. 2025 Apr 30;42(5). doi: 10.1093/molbev/msaf095.
Venom-secreting glands are highly specialized organs evolved throughout the animal kingdom to synthetize and secrete toxins for predation and defense. 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 multispecies 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 specialized functions evolve through gene expression changes. We found that while the venom gland specialized for the mass production of toxins, its homologous glands retained the ancestral digestive functions. The functional divergence and specialization of the venom gland were achieved through a redistribution of its ancestral digestive functions to other organs, specifically the esophagus. 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.
分泌毒液的腺体是动物界进化出的高度特化的器官，用于合成和分泌毒素以进行捕食和防御。毒液因其毒素成分和应用潜力而得到广泛研究；然而，动物如何变得有毒仍知之甚少。因此，毒液系统为理解功能创新背后的分子机制提供了独特的机会。在这里，我们对12种海洋捕食性腹足纲物种进行了多物种多组织比较转录组学分析，包括有毒腺的物种和具有同源非产毒腺体的物种，以研究专门功能如何通过基因表达变化而进化。我们发现，虽然毒腺专门用于大量生产毒素，但其同源腺体保留了祖先的消化功能。毒腺的功能分化和特化是通过将其祖先的消化功能重新分配到其他器官，特别是食管来实现的。这需要整个消化系统协同表达变化并加速转录组进化。毒腺分泌能力的提高是通过调节一种古老的分泌机制，特别是参与内质网应激和未折叠蛋白反应的基因来实现的。这项研究将重点从已充分探索的毒素进化转移到了鲜为人知的毒液产生器官和机制的进化上。因此，它有助于在精细的进化尺度上阐明器官进化背后的分子机制，突出导致功能分化的具体事件。
