Genetic architecture, spatial heterogeneity, and the coevolutionary arms race between newts and snakes

Coevolution between two species can lead to exaggerated phenotypes that vary in a correlated manner across space. However, the conditions under which we expect such spatially varying coevolutionary patterns in polygenic traits are not well-understood. We investigate the coevolutionary dynamics between two species undergoing reciprocal adaptation across space and time, using simulations inspired by the Taricha newt - Thamnophis garter snake system. One striking observation from this system is that newts in some areas carry much more tetrodotoxin than in other areas, and garter snakes that live near more toxic newts tend to be more resistant to this toxin, a correlation seen across several broad geographic areas. Furthermore, snakes seem to be "winning" the coevolutionary arms race, i.e., having a high level of resistance compared to local newt toxicity, despite substantial variation in both toxicity and resistance across the range. We explore how possible genetic architectures of the toxin and resistance traits would affect the coevolutionary dynamics by manipulating both mutation rate and effect size of mutations across many simulations. We find that coevolutionary dynamics alone were not sufficient in our simulations to produce the striking mosaic of levels of toxicity and resistance observed in nature, but simulations with ecological heterogeneity (in trait costliness or interaction rate) did produce such patterns. We also find that in simulations, newts tend to "win" across most combinations of genetic architectures, although the species with higher mutational genetic variance tends to have an advantage.