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An ancient, conserved gene regulatory network led to the rise of oral venom systems

By Agneesh Barua, Alexander S. Mikheyev

Posted 07 Aug 2020
bioRxiv DOI: 10.1101/2020.08.06.240747

Oral venom systems evolved multiple times in numerous vertebrates enabling exploitation of unique predatory niches. Yet how and when they evolved remains poorly understood. Up to now, most research on venom evolution has focussed strictly on the toxins. However, using toxins present in modern day animals to trace the origin of the venom system is difficult, since they tend to evolve rapidly, show complex patterns of expression,an were incorporated into the venom arsenal relatively recently. Here we focus on gene regulatory networks associated with the production of toxins in snakes, rather than the toxins themselves. We found that overall venom gland expression was surprisingly well conserved when compared to salivary glands of other amniotes. We characterized the meta-venom, a network of approximately 3000 non-secreted housekeeping genes that are strongly co-expressed with the toxins, and are primarily involved in protein folding and modification. Conserved across amniotes, this network was co-opted for venom evolution by exaptation of existing members and the recruitment of new toxin genes. For instance, starting from this common molecular foundation, Heloderma lizards, shrews, and solenodon, evolved venoms in parallel by overexpression of kallikreins, which were common in ancestral saliva and include vasodilation when injected, causing circulatory shock. Derived venoms, such as those of snakes, incorporated novel toxins, through still rely on hypotension for prey immobilization. These simmilarities suggest repeated co-option of shared molecular machinery for the evolution oral venom in mammals and reptiles, blurring the line between truly venomous animals and their ancestors. ### Competing Interest Statement The authors have declared no competing interest.

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