Artificial selection for resistance to copper and off-target physiological and behavioral effects in Drosophila melanogaster

Pollution resulting from mining, industry, and agriculture has played an important role in shaping the evolution of diverse organisms. The pathway to evolved resistance can involve polygenic shifts that affect multiple traits. Heavy metal contamination is of particular concern due to the health effects for humans and cross-tolerance effects that influence pesticide resistance. We used a replicated artificial selection approach to examine the response to copper selection in Drosophila melanogaster collected from a retired mine and active fruit orchard. We tracked shifts in resistance to the target trait, copper, as well as off-target effects on cadmium and lead resistance, starvation resistance, lifespan, and feeding aversion to copper contaminated food. Selection for copper resistance increased the focal trait and maintained resistance to non-essential heavy metals while control flies lost metal resistance overtime, implying a cost associated with maintaining resistance to heavy metals. Starvation resistance was correlated with copper resistance, but the correlation was not sufficient to explain the gain in copper resistance. Lifespan was correlated with increased copper resistance in flies collected from one of the two collection sites, suggesting that life history traits may be influenced by repeated heavy metal exposure. Future genomic analysis will help clarify the genetic control of the selection response. Together, our results underscore the complexity of adaptive shift in polygenic traits and provide a basis for further exploration of costs and correlative change following copper selection.