Metabolic stress as a driver of life-history plasticity: flight promotes longevity and antioxidant production in monarch butterflies

Life-history theory predicts that increased investment in traits related to reproduction will be associated with a reduced ability to invest in survival or longevity. One mechanistic explanation for this trade-off is that metabolic stress generated from current fitness activities (e.g. reproduction or locomotion) will increase somatic damage, leading to reduced longevity. Yet, there has been limited support for this damage-based hypothesis. A possible explanation is that individuals can respond to increases in metabolic stress by plastically inducing cellular maintenance responses, which may increase, rather than decrease, longevity. We tested this possibility by experimentally manipulating investment in flight activity (a metabolic stressor) in the migratory monarch butterfly (Danaus plexippus), a species whose reproductive fitness is dependent on survival through a period of metabolically intensive migratory flight. Consistent with the idea that metabolic stress stimulated investment in self-maintenance, increased flight activity enhanced monarch butterfly longevity and somatic tissue antioxidant capacity, likely at a cost to reproductive investment. Our study implicates a role for metabolic stress as a driver of life-history plasticity and supports a model where current engagement in metabolically stressful activities promotes somatic survival by stimulating investment in self-maintenance processes.