Age‐dependent mutational effects curtail the evolution of senescence by antagonistic pleiotropy

One of the two main hypotheses to account for ageing is antagonistic pleiotropy (AP). This model requires alleles that increase vital rates (reproduction or survival) at early age at the expense of vital rates at late age. An important focus of evolutionary studies has been to assess the relative abundance of AP‐type aging alleles that arise through mutation. Here, we develop theory that predicts that senescence per se reduces the probability that these alleles arise by mutation. A direct result is that these mutations should arise with extremely low frequencies in already senescing populations. This has profound implications for the evolution of life histories because it implies that the adaptive evolution of aging via AP will experience negative feedback. This theory also clarifies the previously inexplicable epistatic patterns of genetic covariance across age‐specific vital rates that are observed in mutation accumulation experiments. We show that this epistasis is an emergent property of aging.     

Evolution and ageing

Did senescence evolve as a direct result of natural selection in order to limit the life-span or did increases in longevity evolve in the face of random events that ordinarily limit the life-span? The adaptive hypothesis is that senescence is a programmed process which appeared in evolution because a limited life-span has selective advantages for certain species. Non-adaptive theorists hold that evolution has acted to lengthen the life-span and maximize reproduction and that senescence is only an evolutionary by-product since natural selection does not act directly on postreproductive events. The assumptions and arguments underlying these hypotheses are examined critically in the light of experimental evidence. While theoretical study of the evolution of ageing may advance our understanding of the nature of ageing itself, it is likely that further clarification of the relationship between evolution and ageing will depend on experimental approaches that are now becoming possible.     

Division of labour influences the rate of ageing in weaver ant workers

The evolutionary theory of ageing predicts that the timing of senescence has been primarily shaped by the extrinsic mortality rate, which causes selection intensity to decline over time. One difficulty in testing the evolutionary theory of ageing is that extrinsic mortality risk is often confounded with body size and fecundity, which may also directly affect lifespan. Social insects with a pronounced division of labour between worker castes provide a unique opportunity to study the direct effect of extrinsic mortality on the evolution of ageing rates independently of body size, reproductive effort and genetic configuration. In the weaver ant, Oecophylla smaragdina, the major (large) workers perform the risky tasks outside the nest, while the minor (small) workers stay within the highly protected arboreal nest. Hence, this pronounced division of labour is associated with high differences in extrinsic mortality risks. The evolutionary theory of ageing predicts that the minor workers should have a longer intrinsic lifespan than the major workers. In line with this prediction, we found that in a protected environment the minor workers lived significantly longer than the major workers did. Hence, the ageing rate appears to have been moulded by variation in the extrinsic mortality rate independently of size, reproductive effort and genetic configuration.     

Implications of clonality for ageing research

Senescence, an organismal performance decline with age, has historically been considered a universal phenomenon by evolutionary biologists and zoologist. Yet, increasing fertility and survival with age are nothing new to plant ecologists, among whom it is common knowledge that senescence is not universal. Recently, these two realities have come into a confrontation, begging for the rephrasing of the classical question that has led ageing research for decades: “why do we senesce?” to a more practical “what are the mechanisms by which some organisms escape from senescence?” Plants are amenable to examining this question because of their rich repertoire of life history strategies. These include the existence of permanent seed banks, vegetative dormancy and ability to produce clones, among others. Here, I use a large number of high resolution demographic models from 181 species that reflect life history strategies and their trade-offs among herbaceous perennials, succulents and shrubs measured under field conditions worldwide to examine whether senescence rates of ramets from clonal plants differ from those of whole plants reproducing either strictly sexually, or with a combination of sexual and clonal mechanisms. Contrary to the initial expectation from the mutation accumulation theory of senescence, ramets of clonal plants were more likely to exhibit senescence than those species employing sexual reproduction. I discuss why these comparisons between ramets and genets are useful, as well as its implications and future directions for ageing research.     

Protein networks, pleiotropy and the evolution of senescence

The number of interactions, or connectivity, among proteins in the yeast protein interaction network follows a power law. I compare patterns of connectivity for subsets of yeast proteins associated with senescence and with five other traits. I find that proteins associated with ageing have significantly higher connectivity than expected by chance, a pattern not seen for most other datasets. The pattern holds even when controlling for other factors also associated with connectivity, such as localization of protein expression within the cell. I suggest that these observations are consistent with the antagonistic pleiotropy theory for the evolution of senescence. In further support of this argument, I find that a protein's connectivity is positively correlated with the number of traits it influences or its degree of pleiotropy, and further show that the average degree of pleiotropy is greatest for proteins associated with senescence. I explain these results with a simple mathematical model combining assumptions of the antagonistic pleiotropy theory for the evolution of senescence with data on network topology. These findings integrate molecular and evolutionary models of senescence, and should aid in the search for new ageing genes.     

The evolution of plant life span: facts and hypotheses

There are two different views on the evolution of life forms in Cormophyta: from woody plants to herbaceous ones or in opposite direction - from herbs to trees. In accordance with these views it is supposed that life span in plants changed in the course of evolution from many years (perennials) to few years (annuals, biennials), or went in reverse - from few years to many years. The author discusses the problems of senescence and longevity in Cormophyta in the context of various hypotheses of ageing (programmed death theory, mutation accumulation, antagonistic pleiotropy, disposable soma, genes of ageing, genes of longevity). Special attention is given to bio-morphological aspects of longevity and cases of non-ageing plants ("negative senescence", "potential immortality"). It is proposed to distinguish seven models of simple ontogenesis in Cormophyta that can exemplify the diversity of mechanisms of ageing and longevity. The evolution of life span in plants is considered as an indirect result of natural selection of other characteristics of organisms or as a consequence of fixation of modifications (episelectional evolution). It seems that short life span could emerge several times during evolution of one group of plants, thus favoring its adaptive radiation.     

Post-Meiotic Intra-Testicular Sperm Senescence in a Wild Vertebrate

There is growing interest in sperm senescence, both in its underlying mechanisms and evolutionary consequences, because it can impact the evolution of numerous life history traits. Previous studies have documented various types of sperm senescence, but evidence of post-meiotic intra-testicular sperm senescence in wild animals is lacking. To assess such senescence, we studied within-season changes in sperm motility in the common toad (Bufo bufo), where males produce all sperm prior to the breeding season. We found that males exposed to experimentally induced re-hibernation at the start of the breeding season, that is to experimentally lowered metabolic rates, stored sperm of significantly higher motility than males that were kept under seminatural conditions without females throughout the breeding season. This finding indicates that re-hibernation slows normal rates of sperm ageing and constitutes the first evidence to our knowledge of post-meiotic intra-testicular sperm senescence in a wild vertebrate. We also found that in males kept in seminatural conditions, sperm motility was positively related to the number of matings a male achieved. Thus, our results suggest that post-meiotic intra-testicular sperm senescence does not have a genetically fixed rate and may be modulated by temperature and possibly by mating opportunities.     

Grandmother hypothesis and primate life histories

The adaptive significance of midlife menopause in human females has long engaged the attention of evolutionary anthropologists. In spite of extensive debate, the problem has only recently been examined in the context of primate life histories. Here I extend those investigations by comparing life history traits in 16 primate species to test predictions generated from life history theory. In humans, late ages of maturity and higher than expected birth rates are systematically associated with extended postmenopausal longevity. Links among these adjustments on the primate pattern can explain how selection could slow somatic senescence without favoring extension of the fertile span. This conclusion is consistent with the observation that our fertile spans are similar to those of other pongids. The shape of the argument herein demonstrates the utility of life history theory for solving problems of adaptive evolution in female life history traits, with consequences for broader arguments regarding human evolution.     

Sexual selection and senescence: do seed beetle males (Acanthoscelides obtectus,Bruchidae, Coleoptera) shape the longevity of their mates?

Although the reasons why organisms age and die are generally well understood, it has recently been suggested that an optimal life span has evolved not only as the result of trade‐offs between reproductive performances early and late in life, but also that a balance between the costs and benefits of the number of mating has also played an important role in the evolution of ageing in both sexes. By using four seed beetle (Acanthoscelides obtectus) lines selected for different life history traits, but which have also inadvertently created monoandrous and polyandrous conditions, we showed that males evolved to affect the mortality patterns of females in a way consistent to the postmating sexual selection generated by sexually antagonistic co‐evolution theory. Monoandrous males, irrespectively of body weight and other life history traits specific to their lines, evolved to increase the longevity of control females kept under starvation and suppressed fecundity, compared with males that originated in the lines with effectively polyandrous conditions. When females were allowed to lay eggs, the effects of males from different lines and mating type history on the senescence of females were substantially weaker. We found that males in the line that was evolved to decelerate senescence and polyandrous conditions stimulate the earlier onset of females’ oviposition, relative to males stemmed from the line with accelerated senescence and monoandrous conditions. This fact may explain the absence of difference in the mean longevities between the control females mated to these males and highlight the importance of sexual selection in the evolution of ageing.     

The fitness costs of senescence: The evolutionary importance of events in early adult life

Summary The increased mortality caused by ageing represents a fitness cost to organisms. This paper develops techniques for determining the proportions of that cost that accrue at each age. A variety of analyses using several different sources of data on human ageing—palaeodemographic life tables and life tables from more recent societies with high mortality rates—all suggest that the fitness cost of ageing was high during most of our evolutionary history, and was largely due to physiological changes occurring early in adult life. These results imply that predictions about the nature of senescence based on evolutionary theory should be tested using data from middle-aged individuals. They also have implications about the relative importances for human evolution of the pleiotropy and mutation-accumulation theories of the evolution of senescence, and for the validity of Gompertz Law' for the shape of the relationship between mortality and age. An analysis of a life table of the African buffalo suggests that the costs of ageing early in adult life are relatively high in at least one non-human species in its natural environment.     

The evolutionary ecology of pre- and post-meiotic sperm senescence

Male reproductive success is an extremely variable fitness component. Understanding the maintenance of this variation is a key challenge in evolutionary biology. An often neglected source of variation in male reproductive success is determined by age-dependent patterns of decline in sperm fitness. Two pathways mediate sperm senescence: pre-meiotic senescence of somatic and germ cells of the ageing male, and post-meiotic ageing of the spermatozoon. Recently, theoretical and empirical studies have highlighted wide-ranging implications of both pathways. We clarify different mechanisms of sperm senescence, outlining their distinct evolutionary implications for the male, the female and the zygote, and their influence on fundamental evolutionary processes, including the evolution of anisogamy, sexual conflict, sexual selection, and applied issues such as assisted conception.     

Genetic basis of limited cell proliferation.

Knowledge about the changes that occur as cells traverse their replicative lifespans grows apace, as evidenced by the articles in this issue. Controversy over the interpretation of this knowledge continues, however, and is indeed fuelled by new discoveries (e.g., see Cristofalo, 1990; Holliday, 1990; Smith, 1990). This paper makes a brief commentary on the problems of cellular ageing, with particular emphasis on the unfolding picture of the genetic control of ageing and longevity which derives from evolutionary theory (Kirkwood and Rose, 1991). The case is argued for a synthetic view which recognizes that the immediate causes of limited cell proliferation probably involve some form of active genetic control, but that the ultimate reason for cell ageing is found in evolutionary theories which suggest that the ageing process is not actively programmed and that senescence may be due to the accumulation of damage.     

Early-late life trade-offs and the evolution of ageing in the wild

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing—the disposable soma and the antagonistic pleiotropy theories—and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.     

Why men matter: mating patterns drive evolution of human lifespan

Evolutionary theory predicts that senescence, a decline in survival rates with age, is the consequence of stronger selection on alleles that affect fertility or mortality earlier rather than later in life. Hamilton quantified this argument by showing that a rare mutation reducing survival is opposed by a selective force that declines with age over reproductive life. He used a female-only demographic model, predicting that female menopause at age ca. 50 yrs should be followed by a sharp increase in mortality, a "wall of death." Human lives obviously do not display such a wall. Explanations of the evolution of lifespan beyond the age of female menopause have proven difficult to describe as explicit genetic models. Here we argue that the inclusion of males and mating patterns extends Hamilton's theory and predicts the pattern of human senescence. We analyze a general two-sex model to show that selection favors survival for as long as men reproduce. Male fertility can only result from matings with fertile females, and we present a range of data showing that males much older than 50 yrs have substantial realized fertility through matings with younger females, a pattern that was likely typical among early humans. Thus old-age male fertility provides a selective force against autosomal deleterious mutations at ages far past female menopause with no sharp upper age limit, eliminating the wall of death. Our findings illustrate the evolutionary importance of males and mating preferences, and show that one-sex demographic models are insufficient to describe the forces that shape human senescence.     

On the programmed/non-programmed nature of ageing within the life history

Understanding why and how senescence evolved is of great importance in investigating the multiple, complex mechanisms that influence the course of ageing in humans and other organisms. Compelling arguments eliminate the idea that death is generally programmed by genes for ageing, but there is still a widespread tendency to interpret data in terms of loosely defined 'age regulation', which does not usually make either evolutionary or mechanistic sense. This review critically addresses the role of natural selection in shaping ageing within the life history and examines the implications for research on genetic pathways that influence the life span. It is recognised that in exceptional circumstances the possibility exists for selection to favour limiting survival. In acknowledging that, at least in theory, ageing might occasionally be adaptive, however, the high barriers to validating actual instances of adaptive ageing are made clear.     

Determinants of time allocation across the lifespan

This paper lays the groundwork for a theory of time allocation across the life course, based on the idea that strength and skill vary as a function of age, and that return rates for different activities vary as a function of the combination of strength and skills involved in performing those tasks. We apply the model to traditional human subsistence patterns. The model predicts that young children engage most heavily in low-strength/low-skill activities, middle-aged adults in high-strength/high-skill activities, and older adults in low-strength/high-skill activities. Tests among Machiguenga and Piro forager-horticulturalists of southeastern Peru show that males and females focus on low-strength/low-skill tasks early in life (domestic tasks and several forms of fishing), switch to higher-strength/higher-skill activities in their twenties and thirties (hunting, fishing, and gardening for males; fishing and gardening for females), and shift focus to high-skill activities late in life (manufacture/repair, food processing). Michael Gurven is an assistant professor of anthropology at the University of California-Santa Barbara. He received his Ph.D. from the University of New Mexico in 2000. He has conducted fieldwork in Paraguay and Bolivia with Ache and Tsimane forager-horticulturalists. His research interests include intragroup cooperation and problems of collective action, and the application of life history theory to explaining human longevity, cognitive development, delayed maturation, and sociality. Since 2002, Gurven and Kaplan have co-directed the Tsimane Health and Life History Initiative, a five-year project to develop theory and test implications of different models of human life history evolution. Hillard Kaplan is a professor of anthropology at University of New Mexico. He received his Ph.D. from the University of Utah in 1983. He has conducted fieldwork in Paraguay, Brazil, Botswana, and Bolivia. His research interests include evolutionary perspectives on life course development and senescence, and brain evolution. He has launched theoretical and empirical investigations into each of these areas, uniting evolutionary and economic approaches. He has applied human capital theory toward explaining human life history evolution, and the proximate physiological and psychological mechanisms governing fertility and parental investment in both traditional, high-fertility, subsistence economies and modern, low-fertility, industrial societies.     

Primate longevity: Its place in the mammalian scheme

Data on captive longevity in 587 mammalian species were analyzed in order to evaluate primate longevity in the context of general mammalian life history patterns. Contrary to some recurrent claims in the literature, we found that 1) primates are not the longest-lived mammalian order, either by absolute longevity, longevity corrected for body size, or metabolic expenditure per lifetime; 2) although relative brain size is highly correlated with longevity in primates, this is an aberrant trend for mammals in general, and other body organs account for an even greater amount of variation in longevity; and 3) there has been no progressive evolution of increased longevity among the primate superfamilies. The exceptional magnitude of primate longevity may, in keeping with evolutionary senescence theory, be due to an evolutionary history of low vulnerability to environmentally imposed death due to their body size, arboreal habit, and propensity to live in social groups. © 1992 Wiley-Liss, Inc.     

Reports of the Death of Extrinsic Mortality Moulding Senescence Have Been Greatly Exaggerated

The classic evolutionary theory of aging posits that senescence evolves because the weakening of selection with age allows mutations with late-acting deleterious effects to accumulate. Because extrinsic mortality is an important cause of weakening selection, the central prediction of the theory has been that higher extrinsic mortality should lead to the evolution of a higher rate of senescence. However, the validity of this prediction has been questioned, even to the extent of suggesting that it is not a prediction of the theory at all, primarily on the basis that changes in population growth rate will compensate for changes in extrinsic mortality. The implication is that empiricists have been using the wrong prediction to test the theory. This claim is misleading, however, because it does not apply on an evolutionary timescale, when population size must be roughly constant. With a constant population size, Hamilton’s fitness sensitivities show that extrinsic mortality determines the rate at which the strength of selection declines with age, and thus determines the rate of senescence. The central prediction has been confirmed in the few controlled experiments with model organisms that have been conducted, but clearly this is an area ripe for further investigation.     

Global gradients of avian longevity support the classic evolutionary theory of ageing

Senescence, the process of physiological deterioration associated with growing old, is a shared characteristic of a wide range of animals. Yet, lifespan varies dramatically among species. To explain this variation, the evolutionary theory of ageing has been proposed more than 50 yr ago. Although the theory has been tested experimentally and through comparative analyses, there remains debate whether its fundamental prediction is empirically supported. Here, we use a comprehensive database on avian life history traits to test the evolutionary theory of ageing at a global scale. We show that pronounced geographical gradients of maximum longevity exist, that they are predicted by measures of predator diversity and only partly depend on correlated life‐history traits. The results are consistent with species‐level analyses and can be replicated across bio‐geographical regions. Our analyses suggest that stochastic predation is an important driver of the evolution of lifespan, at least in birds.     

Microsatellites or the eukaryotic genome: life cycle concept and neutrality issues

Microsatellite markers have a great discriminating power. Widely exploited in many disciplines such as forensic science, medical genetics, conservation biology and molecular ecology, they are also used in human population genetics to illuminate our origins. However, strikingly, their fundamental evolutionary mechanisms remain obscure, because of the difficulty of disentangling the complex and numerous factors involved. After a brief summary of their basic characteristics, the concept of life cycle size-dependant is explored. The major mechanisms known to explain the four different phases of their life (conception, birth, growing and senescence/renaissance) are discussed. Emerging questions about their neutrality are also investigated, pointing out a real need to improve our understanding of their mutational dynamics.