Monkeying around with venom: an increased resistance to α-neurotoxins supports an evolutionary arms race between Afro-Asian primates and sympatric cobras

Background Snakes and primates have a multi-layered coevolutionary history as predators, prey, and competitors with each other. Previous work has explored the Snake Detection Theory (SDT), which focuses on the role of snakes as predators of primates and argues that snakes have exerted a selection pressure for the origin of primates’ visual systems, a trait that sets primates apart from other mammals. However, primates also attack and kill snakes and so snakes must simultaneously avoid primates. This factor has been recently highlighted in regard to the movement of hominins into new geographic ranges potentially exerting a selection pressure leading to the evolution of spitting in cobras on three independent occasions. Results Here, we provide further evidence of coevolution between primates and snakes, whereby through frequent encounters and reciprocal antagonism with large, diurnally active neurotoxic elapid snakes, Afro-Asian primates have evolved an increased resistance to α-neurotoxins, which are toxins that target the nicotinic acetylcholine receptors. In contrast, such resistance is not found in Lemuriformes in Madagascar, where venomous snakes are absent, or in Platyrrhini in the Americas, where encounters with neurotoxic elapids are unlikely since they are relatively small, fossorial, and nocturnal. Within the Afro-Asian primates, the increased resistance toward the neurotoxins was significantly amplified in the last common ancestor of chimpanzees, gorillas, and humans (clade Homininae). Comparative testing of venoms from Afro-Asian and American elapid snakes revealed an increase in α-neurotoxin resistance across Afro-Asian primates, which was likely selected against cobra venoms. Through structure-activity studies using native and mutant mimotopes of the α-1 nAChR receptor orthosteric site (loop C), we identified the specific amino acids responsible for conferring this increased level of resistance in hominine primates to the α-neurotoxins in cobra venom. Conclusion We have discovered a pattern of primate susceptibility toward α-neurotoxins that supports the theory of a reciprocal coevolutionary arms-race between venomous snakes and primates.

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

Evidence 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.

Titi monkey neophobia and visual abilities allow for fast responses to novel stimuli

The Snake Detection Theory implicates constricting snakes in the origin of primates, and venomous snakes for differences between catarrhine and platyrrhine primate visual systems. Although many studies using different methods have found very rapid snake detection in catarrhines, including humans, to date no studies have examined how quickly platyrrhine primates can detect snakes. We therefore tested in captive coppery titi monkeys (Plecturocebus cupreus) the latency to detect a small portion of visible snake skin. Because titi monkeys are neophobic, we designed a crossover experiment to compare their latency to look and their duration of looking at a snake skin and synthetic feather of two lengths (2.5 cm and uncovered). To test our predictions that the latency to look would be shorter and the duration of looking would be longer for the snake skin, we used survival/event time models for latency to look and negative binomial mixed models for duration of looking. While titi monkeys looked more quickly and for longer at both the snake skin and feather compared to a control, they also looked more quickly and for longer at larger compared to smaller stimuli. This suggests titi monkeys’ neophobia may augment their visual abilities to help them avoid dangerous stimuli.

Searching for rare and secretive snakes: are camera-trap and box-trap methods interchangeable?

ContextAdvancements in camera-trap technology have provided wildlife researchers with a new technique to better understand their study species. This improved method may be especially useful for many conservation-reliant snake species that can be difficult to detect because of rarity and life histories with secretive behaviours. AimsHere, we report the results of a 6-month camera-trapping study using time lapse-triggered camera traps to detect snakes, in particular the federally listed Louisiana pinesnake (Pituophis ruthveni) in eastern Texas upland forests in the USA. MethodsSo as to evaluate the efficacy of this method of snake detection, we compared camera-trap data with traditional box-trapping data collected over the same time period across a similar habitat type, and with the same goal of detecting P. ruthveni. Key resultsNo differences in focal snake species richness were detected across the trap methods, although the snake-detection rate was nearly three times higher with camera traps than with the box traps. Detection rates of individual snake species varied with the trapping method for all but two species, but temporal trends in detection rates were similar across the trap methods for all but two species. Neither trap method detected P. ruthveni in the present study, but the species has been detected with both trap methods at other sites. ConclusionsThe higher snake-detection rate of the camera-trap method suggests that pairing this method with traditional box traps could increase the detection of P. ruthveni where it occurs. For future monitoring and research on P. ruthveni, and other similarly rare and secretive species of conservation concern, we believe these methods could be used interchangeably by saturating potentially occupied habitats with camera traps initially and then replacing cameras with box traps when the target species is detected. ImplicationsThere are financial and logistical limits to monitoring and researching rare and secretive species with box traps, and those limits are far less restrictive with camera traps. The ability to use camera-trap technologies interchangeably with box-trap methods to collect similar data more efficiently and effectively will have a significant impact on snake conservation.