Every breath you take: assessing metabolic costs of toxin resistance in garter snakes (Thamnophis).

Abstract

Trait specialization often comes at the expense of original trait function, potentially causing evolutionary tradeoffs that may render specialist populations vulnerable to extinction. However, many specialized adaptations evolve repeatedly, suggesting selection favors specialization in specific environments. Some garter snake (Thamnophis) populations possess specialized mutations in voltage-gated sodium channels that allow them to consume Pacific newts (Taricha) defended by a highly potent neurotoxin (tetrodotoxin). These mutations, however, also decrease protein and muscle function, suggesting garter snakes may suffer evolutionary tradeoffs. We measured a key physiological process, standard metabolic rate (SMR), to investigate whether specialized adaptations in toxin-resistant garter snakes affect baseline energy expenditure. In snakes, skeletal muscles influence metabolism and power ventilation, so inefficiencies of sodium channels in these muscles might impact whole-animal energy expenditure. Further, because sodium channels are membrane-bound proteins, inefficiencies of channel kinetics and performance might be exacerbated at suboptimal temperatures. We measured SMR in 2 species, Thamnophis atratus and Thamnophis sirtalis, that independently evolved tetrodotoxin resistance through unique mutations, providing replicate experiments with distinct underlying genetics and potential physiological costs. Despite our expectations, neither resistance phenotype nor sodium channel genotype affected metabolism and resistant snakes did not perform worse under suboptimal body temperature. Instead, T. atratus and T. sirtalis show nearly identical rates of mass-adjusted energy expenditure at both temperatures, despite differing eco-morphologies, life histories, and distant phylogenetic positions. These findings suggest SMR may be a conserved feature of Thamnophis, and that any organismal tradeoffs may be compensated to retain whole-animal function.