Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments

18. Evolution of Aging and Late Life

551 18 EVOLUTION OF AGING AND LATE LIFE Casandra L. Rauser, Laurence D. Mueller, Michael Travisano, and Michael R. Rose EVOLUTIONARY THEORIES OF AGING Hamilton’s Forces of Natural Selection Comparative Biology of Aging Specific Population Genetic Hypotheses for Aging THE ROLE OF EXPERIMENTAL EVOLUTION IN TESTING HAMILTONIAN THEORIES OF AGING Laboratory Evolution of Aging Experimental Population Genetics of Aging EVOLUTIONARY BIOLOGY OF LATE LIFE The Discovery of Late Life Explaining Late Life with Hamiltonian Theory Explaining Late Life with Nonevolutionary Theories Experimentally Testing Hamiltonian Theories of Late Life Experimentally Testing Nonevolutionary Theories of Late Life THE IMPACT OF EXPERIMENTAL EVOLUTION ON AGING RESEARCH Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, edited by Theodore Garland, Jr., and Michael R. Rose. Copyright © by the Regents of the University of California. All rights of reproduction in any form reserved. Aging, like all biological characters, evolves. However, unlike many other biological characters, the evolution of aging is not primarily shaped by powerful natural selection balanced against such mitigating factors as clonal interference, linked deleterious alleles , directional mutation, and the like. Instead, aging is evolutionarily distinctive because it arises from the progressive fall in Hamilton’s forces of natural selection acting on the survival and reproduction of the somata of ovigerous species (Hamilton 1966; Rose et al. 2007). Therefore, the evolutionary mechanisms underlying aging are different from those underlying most other phenotypes. That is, aging does not have a function or purpose, nor is it adaptive. Thus, aging must be studied from a different theoretical and experimental perspective than other biological characteristics. From an evolutionary point of view, aging can be defined as a sustained age-specific decline of fitness-related characteristics, such as survival probability and fertility, that is not due to external environmental factors like disease , predation, or climate. Indeed, experimental evolutionary approaches to the problem of aging have mainly focused on manipulating and measuring age-specific survival probability and age-specific fecundity. Experimental evolution has played an important role in aging research over the last few decades. However, the success of the experimental evolution approach in aging research is in large part due to the availability of a well-developed body of evolutionary theory that concerns aging (see also Mueller this volume). This strong theoretical foundation has provided experimental evolutionary biologists with relatively straightforward predictions to test. Nonetheless, the evolutionary biology of aging would not have progressed as it has over the last few decades without the relatively clear results obtained from some remarkably repetitious, if not dreary, experimental work. In this chapter, we discuss the evolutionary theories of aging and the experimental studies that have tested and, in a few cases, challenged these theories. We also discuss the postaging phase of life, referred to here as “late life,” and the experimental and theoretical work surrounding this phenomenon. The discovery, explanation, and manipulation of late life have served to put the evolution of aging into a strikingly different context. However, we will also discuss a variety of dissenting views, ranging from biomedically motivated research with large-effect mutants to anti-Hamiltonian research by demographers. As we will explain in detail, we regard much of this work as positively misleading with respect to how and why aging evolves. EVOLUTIONARY THEORIES OF AGING Although the evolution of aging was discussed in the nineteenth century by Alfred Russel Wallace and August Weismann, it was not until the advent of theoretical population genetics in the twentieth century that the evolutionary analysis of aging was made relatively coherent (Rose 1991). In early discussions of aging, a few evolutionary biologists erroneously proposed that aging evolved to eliminate older individuals to make way 552 • A P P L I C A T I O N S for the young (e.g., Weismann 1891). This is an idea that is still repeated to this day, at least by some authors without training in evolutionary theory. The key mistake common to all these proposals is that they presume that, without aging, there would be an abundance of frail older organisms in natural populations. However, for the vast majority of species in the wild, this is not likely to be the case because disease, starvation, predation, accident, and bad weather normally remove most individuals from wild populations before significant aging has occurred (Medawar 1952), the most important exceptions being species that have benefited from human interventions, including humans themselves , our pets, zoo animals, laboratory model organisms, and...