Convergent evolution of venom gland transcriptomes across Metazoa

Abstract

Animals have repeatedly evolved specialized organs and anatomical structures to produce and deliver a cocktail of potent bioactive molecules to subdue prey or predators: venom. This makes it one of the most widespread convergent functions in the animal kingdom. Whether animals have adopted the same genetic toolkit to evolved venom systems is a fascinating question that still eludes us. Here, we performed the first comparative analysis of venom gland transcriptomes from 20 venomous species spanning the main Metazoan lineages, to test whether different animals have independently adopted similar molecular mechanisms to perform the same function. We found a strong convergence in gene expression profiles, with venom glands being more similar to each other than to any other tissue from the same species, and their differences closely mirroring the species phylogeny. Although venom glands secrete some of the fastest evolving molecules (toxins), their gene expression does not evolve faster than evolutionarily older tissues. We found 15 venom gland specific gene modules enriched in endoplasmic reticulum stress and unfolded protein response pathways, indicating that animals have independently adopted stress response mechanisms to cope with mass production of toxins. This, in turns, activates regulatory networks for epithelial development, cell turnover and maintenance which seem composed of both convergent and lineage-specific factors, possibly reflecting the different developmental origins of venom glands. This study represents the first step towards an understanding of the molecular mechanisms underlying the repeated evolution of one of the most successful adaptive traits in the animal kingdom.

Venom gland organogenesis in the common house spider

“…3). sum-1 had the highest FC, and its specificity to venom glands has been observed in other spider species 22 . forkhead box C1-A displayed a similar pattern, with venom gland-specific expression in both juveniles and adults (Fig.…”

“…sum-1 is orthologous to the Drosophila gene nautilus , and to the mammalian family of bHLH myogenic regulatory factors involved in muscle differentiation 31 . In other venomous animals, the myogenic factors myf5 or myod1 were found to be expressed in venom glands, albeit at low levels and not in a tissue-specific manner 22 . This suggests that the specificity of sum-1 in the muscle fibres surrounding the glandular tissue may be restricted to spiders.…”

“…In particular, sage expression was confined to the glandular epithelium across all developmental stages, underscoring the significance of this transcription factor for the development and maintenance of venom glands. sage orthologs have been previously found to be upregulated in venom glands of various spider species and scorpions 22 . In insects, sage is expressed in robber flies' thoracic (i.e., venom) glands but not in hymenopteran venom glands 22 , the latter being evolutionary linked to the reproductive system 36 .…”

“…sage orthologs have been previously found to be upregulated in venom glands of various spider species and scorpions 22 . In insects, sage is expressed in robber flies' thoracic (i.e., venom) glands but not in hymenopteran venom glands 22 , the latter being evolutionary linked to the reproductive system 36 . These observations suggest an evolutionary link between the venom gland and salivary, or any other prosomal gland, that might have been present in the arachnid ancestor.…”

The perspective of fish venom: An overview of the physiology, evolution, molecular and genetics

“…The selective expression of venom peptides or proteins from the genes may cause these discrepancies. Also, sometimes enough venom in a single venom gland may lead to retrieving venom samples for nextgeneration sequencing in a single while proteomic material is only gathered from the other group (Xie et al, 2017;Lopes-Ferreira et al, 2022;Zancolli et al, 2022).…”