How universal is the evolution of senescence?

Review of: Shefferson, Richard P., Jones, Owen R., and Salguero‐Gomez R., eds. 2017. The evolution of senescence in the tree of life. Cambridge Univ. Press, Cambridge, U.K. 402pp. ISBN 978–1107078505; $70 HB. Senescence, or the process of somatic deterioration with advancing age, is one of the major puzzles of evolutionary theory. Since senescence is caused by many mechanisms, and can occur for a variety of reasons, reliably identifying and describing patterns of senescence can be difficult. Nevertheless, the study of aging is a productive and rapidly growing field of research: aging is now studied in a wide variety of taxa, and on every biological level from genomes to populations. Taking stock of where this discipline is headed is thus no small feat. The Evolution of Senescence in the Tree of Life is a well‐written volume that discusses major questions concerning senescence and critically assesses the theories purporting to answer them. Since Peter Medawar developed the idea of mutation accumulation, we have had evolutionary explanations of senescence (Medawar ). The Evolution of Senescence in the Tree of Life aims to call into question the prevailing evolutionary explanations of biological senescence by asking two questions. First, how universal is senescence? Second, what are the proposed “universal evolutionary mechanisms” that are supposed to underlie the physiological, genetic, and demographic patterns of senescence in each and every organism? The book, which is as rich in empirical data as it is in theoretical detail, reports the state of the contemporary theories of the evolution of senescence, none of which seem to apply consistently across the tree of life. The main evolutionary theories of senescence should be familiar to most biologists. The mutation accumulation hypothesis suggests that patterns of senescence arise as deleterious mutations—whose harmful effects are realized only late in life—are accumulated over generations (see Medawar ; Williams , ; Hamilton ). The antagonistic pleiotropy hypothesis emphasizes that senescence can be explained by the accumulation of traits (or genes) with benefits realized early in life, but costs realized late in life. Williams’ hypothetical example was calcium deposition in humans: he reasoned that higher calcium retention and deposition might have positive fitness benefits early in life, because of increased bone strength, but could also shorten lifespan by inadvertently promoting artery calcification. The disposable soma hypothesis is broadly compatible with both genetic‐level explanations of senescence, and suggests that organisms must budget finite energy resources between maintenance and reproduction (Kirkwood ; Kirkwood and Holliday ). This tradeoff implies that, in any organism, there is a point at which investing more resources in maintenance does not realize higher fitness gains than would investing the same resources in producing additional offspring. The functions of the “disposable soma” and germ cells are therefore different; somatic maintenance costs must be minimized to maximize the reproductive potential of the germline. Each of these evolutionary theories of senescence, as well as their contemporary theoretical refinements, is explained in greater detail in the book, where their proponents also provide exhaustive and up‐to‐date replies to critics. The editors of the volume consistently argue that the “universal” theories of the evolution of senescence face two important challenges. First, the abstract assumptions that are often made by explanatory models are too simple to be universal: for instance, distinguishing between “germ” and “soma” is useful when discussing animals, but is less so when considering some plants or fungi. Second, there is abundant empirical evidence that some organisms show negligible (or even negative) senescence (e.g., Hydra spp., lobsters, rockfish, aspen). If senescence is absent from even one clade, it must not be universal. This focus on the universality of senescence is what is novel about this book: here the editors’ thesis is that the study of senescence has freed itself from one sort of problem—that of basing the empirical study of senescence on idiosyncratic data from a very few clades (primarily mammals and birds)—only to find itself facing a new one: a lack of universal applicability and, consequently, unreliable quantitative predictions. The text of the book itself is divided into subsections. An introductory section explains the evolutionary theories of aging in detail. The next three sections address these theories by introducing empirical work, but from three distinct clades: animals, plants, and fungi. These chapters contribute to book's main discussion of the evolution of senescence, but will probably also interest readers interested in other life‐history traits. Chapter 6 discusses human senescence, where the author makes two key points: first, he notes that humans have patterns of senescence that differ from those found in other animals, thus calling into question the predictions of the major evolutionary theories of senescence. Second, he argues that density‐ and condition‐dependent factors may be relatively more important for understanding human aging than in understanding aging in other animal species. The final section contains a single chapter—perhaps the most interesting in the book—that examines the degree to which life‐history tradeoffs consistently affect rates of senescence across the whole Tree of Life. Such scope is not common in studies of aging in the literature, and its inclusion is welcome here. Another valuable feature of this book is that it uses terminology carefully and consistently. For instance, very early on the editors define “senescence” as a “process of physiological or biological decay leading to increasing mortality rates and/or decreasing fertility with age,” and contrast this with “aging,” which they define as “the march of time, with no physiological decay implied” (p. 17). This is useful for two reasons: first, it is simply necessary to get the facts straight and avoid confusion. This is a major source of confusion elsewhere in the literature, where clinical studies of aging in humans or mice use terms somewhat differently than articles published in evolutionary ecology journals do. Second, the evolutionary explanations discussed in the book are based on the study of different levels of biological organization—that is the genetic level or the organismal level—and must share definitions to be universal. The editors also identify five “particularly important venues of research” (p. 20) to act as focal points for future studies of the evolution of senescence. First, they argue that future studies should work to reconcile the two ways in which senescence is studied: as “actuarial senescence,” the demographic study of age‐specific mortality rates of populations, and as “mechanistic senescence,” which focuses on the “physiochemical processes that lead to decay, such as oxidative stress” (p. 21). Second, the editors believe that some life histories can confound the study of senescence (e.g., long‐lived perennial plants). Moreover, long‐lived clonal organisms with negligible senescence—such as quaking aspen—are curious outliers that are especially likely to yield insight into how senescence can be delayed or avoided. Third, future studies of senescence should prioritize the collection of examples of senescence in the wild, where data is relatively sparse and—when it is available—rarely agrees with theoretical predictions. The editors suggest that combining controlled lab and in situ field experiments in parallel should be an important priority. Fourth, the editors argue that extrinsic (environmental) mortality risks are likely to be more important for the evolution of senescence than is currently accepted, and that the “Hamiltonian framing” of current theories of the evolution of senescence causes researchers to overemphasize intrinsic causes of mortality. Finally, the editors believe that the study of senescence should incorporate more phylogenetic data. This is not only to develop a broader comparative framework for the study of senescence, but also to test whether patterns of senescence have macroevolutionary implications or not. In conclusion, I was pleasantly surprised by reading The Evolution of Senescence in the Tree of Life—this volume highlighted both the reasons that the mutation accumulation, antagonistic pleiotropy, and disposable soma theories are still taken seriously as evolutionary explanations of senescence, as well as what the most relevant empirical and theoretical challenges to them are. The authors of many of the contributed chapters are preeminent experts on their topics, and the chapters are without exception well written. Part of the excitement of reading this book is the realization of just how unfinished the task of creating a general evolutionary explanation of aging is. The only thing that I missed was a review of the theory and mechanisms regulating programmed cell death across the Tree of Life: this omission seemed odd given how active this area of research is, even if much of it is clinical rather than ecological, and how theoretically significant the possibility of ubiquitous programmed cell death is. This, however, does not overshadow the achievement of the editors in compiling an interesting and accessible review of the state of the study of senescence. The volume shines as an example of a contributed volume with a sharp, timely thesis aimed at changing the outlook of a field of research, and is likely to be appreciated by anyone with an interest in the study of aging and/or senescence. P.W.H. read the book and wrote this review alone. I would like to thank Amanda Feeney for her constructive feedback during the preparation of this manuscript, and NSERC and the Alexander von Humboldt Foundation for funding this research. This research was supported by a Natural Sciences and Engineering Research Council (NSERC) Postdoctoral Fellowship and an Alexander von Humboldt Foundation Research Fellowship. Associate Editor: L. Delph Handling Editor: M. Noor

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