Coevolution between primates and venomous snakes revealed by α-neurotoxin susceptibility

Abstract

AbstractEvidence suggests venomous snakes and primates have evolved certain traits in response to a coevolutionary arms-race. In both clades, evolved traits include an increase in brain size and enhanced vision. Lineage specific traits include in primates an inherent fear of snakes, while cobras have evolved defensive toxins, hooding, aposematism and venom spitting. To strengthen the claims of coevolution between venomous snakes and primates, more evidence of coevolved traits is needed to highlight the importance of this arms-race. We report a significantly reduced susceptibility of snake venom α-neurotoxins toward the α-1 nicotinic acetylcholine receptor orthosteric site within the catarrhine primates. This trait is particularly amplified within the clade Homininae. This relationship is supported by post-synaptic neurotoxic symptoms of envenoming relative to prey species being much lower humans due to weak binding of α-neurotoxins to human nicotinic receptors. Catarrhines are sympatric with many species of large, diurnal, neurotoxically venomous snakes and as such are likely to have had a long history of interaction with them. Conversely, the Lemuriformes and Platyrrhini are highly susceptible to binding of α-neurotoxins, which is consistent with them occupying geographical locations either devoid of venomous snakes or areas with neurotoxic snakes that are small, fossorial, and nocturnal. These data are consistent with the snake detection theory in that they follow a similar pattern of evolved traits within specific primate clades that are sympatric with venomous snakes. These results add new strong evidence in support of snakes and primates coevolving through arms-races that shaped selection pressures for both lineages.Significance StatementWe have discovered a pattern of primate susceptibility towards α-neurotoxins that supports the theory of a coevolutionary arms-race between venomous snakes and primates.