The Role of Senescence in Life History Evolution

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9707473 Reznick Most current research on the aging process evaluates the influence of environmental factors on the rate of aging or characterizes individual genes that influence lifespan in two model organisms, the nematode Caenorhabditis elegans and the fruitfly Drosophila melanogaster. We propose evaluating aging instead from an evolutionary perspective. Senescence is thought to have evolved because the strength of selection declines with an individual's age; natural selection will have the greatest influence on individuals that are early in their reproductive lifespans because they have only begun to contribute offspring to the next generation. The influence of selection declines to zero when individuals are no longer reproducing or caring for offspring. Two genetic mechanisms, mutation accumulation and antagonistic pleiotropy, can account for the evolution of senescence due to this age-specific decline in the strength of selection. Both mechanisms predict that high extrinsic mortality rates will select for earlier senescence. "Extrinsic mortality" refers to death to external causes, such as predation. We will test this prediction by evaluating the lifespan and lifetime reproductive performance of guppies derived from high and low predation environments. In our earlier work, we established that natural populations of guppies from Trinidad experience high versus low mortality rates, correlated with the species of predators present. Guppies from high predation environments mature at an earlier age, smaller size, and devote more of their resources to reproduction than their counterparts from low predation environments. These differences were shown to have a genetic basis. They were further evaluated by modifying mortality rates in natural populations, resulting in the evolution of these same life history patterns over time intervals as short as four years. These combined studies argue that predators and mortality rates have selected for changes in the early life history, or that the differences that we observed among populations in early life history represent an adaptation to prevailing mortality rates. These results provide the rationale for predicting that predation has also influences the evolution of the aging process.! Evaluating aging in these fish potentially provides a new model system for studying the aging process, a new way of identifying genes associated with aging, and a means for answering a question that is not accessible in all lab-based systems considered thus far, which is "why do we see such dramatic differences in lifespan among species in nature?".