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Investigation of the Pallid Bat’s (Antrozous pallidus) Resistance to Scorpion Venoms

Abstract

The pallid bat (Antrozous pallidus), a gleaning bat found in the western United States and Mexico, hunts a wide variety of ground-dwelling prey, including scorpions. Anecdotal evidence suggests that the pallid bat is resistant to scorpion venom, but no systematic study has been performed. Here we show with behavioral measures and direct injection of venom that the pallid bat is resistant to venom of the Arizona bark scorpion, Centruroides sculpturatus. Our results show that the pallid bat is stung multiple times during a hunt without any noticeable effect on behavior. In addition, direct injection of venom at mouse LD50 concentrations (1.5 mg/kg) has no effect on bat behavior. At the highest concentration tested (10 mg/kg), three out of four bats showed no effects. One of the four bats showed a transient effect suggesting that additional studies are required to identify potential regional variation in venom tolerance. Scorpion venom is a cocktail of toxins, some of which activate voltage-gated sodium ion channels, causing intense pain. Dorsal root ganglia (DRG) contain nociceptive neurons and are principal targets of scorpion venom toxins. To understand if mutations in specific ion channels contribute to venom resistance, a pallid bat DRG transcriptome was generated. As sodium channels are a major target of scorpion venom, we identified amino acid substitutions present in the pallid bat that may lead to venom resistance. Some of these substitutions are similar to corresponding amino acids in sodium channel isoforms responsible for reduced venom binding activity. The substitution found previously in the grasshopper mouse providing venom resistance to the bark scorpion is not present in the pallid bat, indicating a potentially novel mechanism for venom resistance in the bat that remains to be identified. Taken together, these results indicate that the pallid bat is resistant to venom of the bark scorpion and altered sodium ion channel function may partly underlie such resistance.The pallid bat (Antrozous pallidus) is a gleaning bat found in western North America and is a well known hunter of scorpions. Previous work has shown the pallid bat is highly resistant to the venom of the Arizona barks scorpion, Centruroides sculpturatus. Here we build upon that work and show how the pallid bat may overcome the venom via cellular and genetic adaptations. Pallid bats were injected with doses of C. sculpturatus venom up to 20 mg/kg and showed only minor symptoms and made full recoveries. The serum neutralizing effects of pallid bat blood serum was tested via incubation of pallid bat blood serum with the venom before injection into mice. The serum incubated venom retained equivalent potency as the non-serum-incubated venom suggesting the pallid bat does not inactivate the venom via serum-based mechanisms. The sensory neurons in pallid bat dorsal root and trigeminal ganglia were tested via the Constellation Pharmacology method. Pallid bat sensory neurons experienced more calcium signal when challenged with C. sculpturatus venom than mouse sensory neurons, suggesting pallid bat venom resistance is not dependent on preventing increases in somatic calcium concentrations. The sequences of two voltage gated sodium channels were compared to other species and possible sites influencing venom action showed signs of positive selection in scorpion hunting bats.

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