Understanding Patterns of Resistance to Spider Venom in Lizards: Ecology and Phylogeny Matter

Abstract

Lizards and spiders often engage in predator-prey interactions, and many spiders can be dangerous as both predator and prey. However, we know little about how lizards tackle dangerous spider prey. And yet, some species are known to consume especially potent spider prey, like the western black widow (Latrodectus hesperus). In particular, Elgaria multicarinata is known to preferentially consume venom-defended L. hesperus. I asked whether E. multicarinata possessed resistance to the venom of L. hesperus and evaluated resistance at two levels of biological organization: at the whole animal level, and at the muscle tissue level. I included one other sympatric species that will eat L. hesperus when offered (Sceloporus occidentalis), and one sympatric species that is known prey of L. hesperus (Uta stansburiana). To evaluate the whole animal resistance, I used sprint speed performance; to evaluate muscle tissue resistance, I used comparative histology. Lizards were tested against either a control (sterile saline), “low” (1 mouse LD50), or “high” (5 mouse LD50) dose of black widow spider venom (BWSV). I found that E. multicarinata showed no response to any venom treatment, while U. stansburiana had tissue level responses for both low and high venom treatments and a whole animal response only for high venom treatment; S. occidentalis was somewhere in the middle, with no whole animal response and slight (but significant) muscle tissue response.Given the variety of responses in these three lizards across response levels (whole animal, tissue) and treatments (low, high), and the lack of drastic susceptibility in U. stansburiana, I then asked whether resistance to BWSV could be rooted deep in the squamate lineage (i.e. an ancestral trait of all lizards). I investigated this by testing for whole animal and muscle tissue resistance to BWSV using sprint speed performance and comparative histology on species representing a broader phylogenetic, ecological, and geographical scope of Squamate taxa. I found that insectivorous species (Coleonyx variegatus and Takydromus sexlineatus) were resistant to both low and high venom treatments at the whole animal, but not at the tissue level. I included a single herbivorous species, Iguana iguana, which showed drastic decreases in sprint performance and severe tissue responses for both low and high venom treatments. The variation in responses seen at different levels (whole animal, tissue) and at different treatments (low, high) combined with ecological traits, provides evidence that both ecology and phylogeny contribute to whether BWSV resistance is present, and at what level – whole animal and/or muscle tissue.