Tracing Monotreme Venom Evolution in the Genomics Era

Abstract

The monotremes (platypuses and echidnas) represent one of only four extant venomous mammalian lineages. Until recently, monotreme venom was poorly understood. However, the availability of the platypus genome and increasingly sophisticated genomic tools has allowed us to characterize platypus toxins, and provides a means of reconstructing the evolutionary history of monotreme venom. Here we review the physiology of platypus and echidna crural (venom) systems as well as pharmacological and genomic studies of monotreme toxins. Further, we synthesize current ideas about the evolution of the venom system, which in the platypus is likely to have been retained from a venomous ancestor, whilst being lost in the echidnas. We also outline several research directions and outstanding questions that would be productive to address in future research. An improved characterization of mammalian venoms will not only yield new toxins with potential therapeutic uses, but will also aid in our understanding of the way that this unusual trait evolves.

The platypus: evolutionary history, biology, and an uncertain future

“…The venom disrupts hemostasis (Martin and Tidswell 1895; Kellaway and Le Messurier 1935), cell membranes (Kourie 1999; Torres et al 2002a), and nociception (Kourie 1999; de Plater et al 2001). Venom may have a primarily reproductive function, when males fight each other over access to breeding females, as indicated by cyclic venom production (Temple-Smith 1973; Whittington and Belov 2014) and fresh spur wounds and possible temporary partial paralysis in envenomated males during the breeding season (Fleay 1950; Temple-Smith 1973). Spur wounds heal, indicating that intraspecific envenomation hampers or temporarily disables competitors; death has been recorded only in captive conditions due to multiple spurring (Temple-Smith 1973; Grant and Fanning 2007).…”

“…The venom causes excruciating local pain in humans that can effectively be reduced using a nerve blocker (Temple-Smith 1973; Fenner et al 1992). Platypus venom may provide clinically useful substances and improve understanding and treatment of novel pain pathways (Fenner et al 1992; Whittington and Belov 2014, 2016).…”

Evaluation of the physiological activity of venom from the Eurasian water shrew Neomys fodiens

“…Additionally, according to recent research, three species of vampire bats (Chiroptera) and three species of lorises (Primates) are considered venomous as well [ 5 , 9 – 11 ]. Only the platypus venom has been comprehensively studied with a focus on its composition, function and evolution [ 12 ]. Some studies on toxic components and function of the vampire bat and loris (especially the slow loris) venom have been performed [ 10 , 11 ].…”

Cabinet of Curiosities: Venom Systems and Their Ecological Function in Mammals, with a Focus on Primates

“…Advances in genomic techniques, and proteomic and biochemical analyses helps to identify new toxins, shed light on their evolution, and answer questions like when in evolutionary history venom genes have been recruited, got retained and lost in mammals and other taxa [ 95 ]. Using the fact that the composition of venom can vary within one species and even individuals [ 94 , 95 , 96 ] may further help us to study venoms.…”

“…Advances in genomic techniques, and proteomic and biochemical analyses helps to identify new toxins, shed light on their evolution, and answer questions like when in evolutionary history venom genes have been recruited, got retained and lost in mammals and other taxa [ 95 ]. Using the fact that the composition of venom can vary within one species and even individuals [ 94 , 95 , 96 ] may further help us to study venoms. Recent research on platypus venom for instance has used the completely sequenced genome in combination with next-generation sequencing of a gland transcriptome during the passive (non-venomous) and active (venomous) season to identify new toxins including five that are only known from platypus [ 95 ] and to reveal that not only gene duplication, but also mutations in regulatory or coding regions and alternate splicing [ 6 ].…”