Limits to the adaptation of herbivorous spider mites to metal accumulation in homogeneous and heterogeneous environments

Metal accumulation is used by some plants as a defence against herbivores. Yet, herbivores may adapt to these defences, becoming less susceptible. Moreover, ecosystems often contain plants that do and do not accumulate metals, and such heterogeneity may affect herbivore adaptation. Surprisingly, few studies have tested this. Tomato plants accumulate cadmium, affecting the performance of the herbivorous spider mite Tetranychus evansi. Here, we performed experimental evolution to test whether these mites adapt to plants with high cadmium concentrations, in homogeneous (plants with cadmium) or heterogeneous (plants with and without cadmium) environments. We measured fecundity, hatching rate and the number of adult offspring after 12 and 33 generations and habitat choice after 14 and 51 generations, detecting no trait change, which implies absence of adaptation. We then tested whether this absence of adaptation was due to a lack of genetic variation in the traits measured and, indeed, additive genetic variance was low for the measured traits. Possibly, we did not measure the traits that contributed to population persistence on plants with cadmium. Interestingly, despite no signs of adaptation we observed a decrease in fecundity and number of adult offspring produced in cadmium-free plants, in the populations evolving in environments with cadmium. Being this the case, evolving in environments with cadmium may reduce the growth rate of spider mite populations on non-accumulating plants as well. Nevertheless, adaptation to metal accumulation may occur via herbivore traits not commonly measured, which calls for broader studies on this topic.