Geographic Range Size Predicts Butterfly Species' Tolerance to Heavy Metals More Than Evolutionary History With Toxic Larval Diets

Abstract

Some organisms appear to thrive in contaminated environments, while others are more sensitive, though the causes of this variation are unclear. The toxin coevolution hypothesis posits that an evolutionary history with natural toxins preadapts species to deal with novel toxins, while the range-size-tolerance hypothesis posits that a larger geographic range selects for broader tolerance to stressors. Butterflies are a prime system to investigate these hypotheses because they are diverse, feed on a range of larval host plants that vary in defensive compounds, and many are found in polluted environments. We ask how these hypotheses explain varying tolerance to heavy metal pollution, measured here as loads of four heavy metals along an urban gradient of metal exposure. We compared 26 butterfly species that vary in their evolutionary history with mutagenic plant defensive chemicals as well as their geographic range size. We built a dataset of plant mutagenicity synthesizing 40 years of standardized mutagenicity screening in plants, including 502 plant species of 103 families within 37 orders. We used this dataset, coupled with butterfly host records, to estimate evolutionary history with mutagens. We found that butterfly species with larger ranges tolerated significantly greater concentrations of lead, arsenic, and cadmium in their tissues. Additionally, species with a history of feeding on relatively more mutagenic host plant families tolerated greater maximum lead concentrations in their thoracic tissue. This research provides additional support for the growing observation that small-ranged species are more vulnerable to environmental change, in this case, metal pollution. In addition, an evolutionary history with mutagenic host plants may provide some additional resilience, although less than geographic range size. In addition, our dataset on comparative plant mutagenicity will facilitate future research on plant-herbivore coevolution, in fields such as chemical, community, and urban ecology.