The theory that trade-offs exist between longevity and performance is a pervasive paradigm in analyses of life-history evolution. However, in the case of the naturally occurring indy mutant Drosophila, lifespan has been doubled without decreases in fitness; these flies are both healthy and fertile during their entire lives. The name indy is short for mutations in a gene named I'm not dead yet, which encodes a protein that transports Krebs cycle intermediates needed for intermediary metabolism. The performance trade-offs in long-lived indy flies will only be present in the flies when food is scarce, as a reduction of INDY protein expression levels reduces the efficiency by which the insect utilises calories from food.

Marden and co-authors hypothesized that performance trade-offs in indy flies may be conditional and may depend on levels of environmental stress, including the quality and quantity of food available. To test this hypothesis, the authors measured mortality rates, metabolic rates,flight performance, fecundity and eclosion in two independent indymutant strains of fly under normal conditions and when the flies' caloric intake was restricted.

The team measured mortality rates for well-fed wild-type and mutant flies at 25°C and confirmed that all of the indy mutant flies had significantly lower mortality rates than the rates for normal-lifespan flies. Metabolic rates of flies were measured by CO2 emissions of resting flies in flow-through respirometry chambers. There was no indication of any significant difference between the metabolic rates of indy mutant and normal-lived flies, although the flies' measured metabolic rates were affected by temperature, respirometry chamber, body mass and fly age. Marden and co-workers also assessed the flies' performances by measuring their flight velocities from three-dimensional video recording of flight paths and found no significant differences between flight velocities of the two indymutant strains and the two normal-lived strains.

Having established that there appeared to be no trade-off between a variety of physiological traits and the mutant flies' longevity, the team tested the insect's reproductive fitness under normal circumstances and stressful conditions. Age-specific fecundity was determined by counting the daily egg production rate of individual females. Under high calorie conditions, indy mutant flies were significantly more fecund than normal-lived flies. However, when the indy mutant flies were reared on a calorie-restricted diet, their fecundity fell. This pattern held for eclosion as well; greater numbers of adults eclosed from indy mutant fly eggs than from normal life expectancy fly eggs under normal conditions, while fewer indy mutant eggs hatched under low-calorie conditions. Under stressful conditions, the mutant flies had traded off fertility in return for a greater life expectancy.

These results suggest that trade-offs between lifespan and performance in indy mutant flies exist, but that they are conditional and dependent on food availability. Although long-lived indy mutant strains will have an advantage over wild-type flies under normal circumstances, spatial and temporal variation in the quality and quantity of nutritional resources may be great enough to decrease the fitness of natural indy mutant flies,preventing them from swamping the wild-type population. Thus, the ability to eat well will have an impact on life-history evolution in this naturally occurring mutant population.

Marden, J. H., Rogina, B., Montooth, K. L. and Helfand, S.(
). Conditional tradeoffs between aging and organismal performance of indy long-lived mutant flies.
Proc. Natl. Acad. Sci. USA