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Williams’ evolutionary theory of senescence based on antagonistic pleiotropy has become a landmark in evolutionary biology, and more recently in biogerontology and evolutionary medicine. In his original article, Williams launched a set of nine “testable deductions” from his theory. Although some of these predictions have been repeatedly discussed, most have been overlooked and no systematic evaluation of the whole set of Williams’ original predictions has been performed. For the sixtieth anniversary of the publication of the Williams’ article, we provide an updated evaluation of all these predictions. We present the pros and cons of each prediction based on recent accumulation of both theoretical and empirical studies performed in the laboratory and in the wild. From our viewpoint, six predictions are mostly supported by our current knowledge at least under some conditions (although Williams’ theory cannot thoroughly explain why for some of them). Three predictions, all involving the timing of senescence, are not supported. Our critical review of Williams’ predictions highlights the importance of William’s contribution and clearly demonstrates that, 60 years after its publication, his article does not show any sign of senescence.

Senescence—the decline in age‐specific contribution to fitness with increasing age—has been widely investigated in evolutionary ecology. A tremendous amount of detailed empirical analyses have now revealed the widespread occurrence of demographic senescence (i.e. both actuarial and reproductive senescence) and have started to identify factors (e.g. environmental conditions) that modulate its timing and intensity, both within and across species. In this special feature, we have built on this flourishing work to highlight several axes of research that would benefit from more integrative and multidisciplinary approaches. Several contributions compiled in this special feature emphasize that our understanding of senescence remains taxonomically limited, mostly focused on birds and mammals, and is therefore not representative of the biological diversity displayed across the tree of life. In line with this observation, the influence of some peculiar lifestyles (e.g. involving sociality or modularity) on the evolution of senescence is yet to be deciphered. Understanding of the diversity of senescence patterns across and within species and among traits will necessitate the establishment of new metrics as a golden standard to fully account for age‐specific changes recorded in individuals’ performance. This is illustrated with the specific case of actuarial senescence. This special feature also highlights that the diversity of biological samples collected from wild plants and animals, along with accurate demographic data, is expanding. The fast development of new molecular tools now offers a unique opportunity to launch research programmes at the interface of physiology, health and ageing in non‐model organisms. We argue that while these different research axes constitute key avenues of investigations for the coming years, they are only the tip of the iceberg. To appreciate the full complexity of the senescence process in nature, from its evolutionary causes to its demographic consequences, we also need a better understanding of the role played by both environmental conditions and gene–environment interactions, of constraints, and of senescence, an improved assessment of the influence of individual heterogeneity, and the consideration of transgenerational effects when quantifying the fitness consequences of senescence.

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female’s median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast–slow life‐history continuum. As there are few long‐term datasets of wild populations with known‐age individuals, intraspecific (i.e. between‐population) variation in senescence is understudied and limited to comparisons of wild and captive populations of the same species, mostly birds and mammals. In this paper, we examined how population position along the fast–slow life‐history continuum affects intraspecific variation in senescence in an amphibian, Bombina variegata. We used capture–recapture data collected in four populations with contrasting life‐history strategies. Senescence trajectories were analysed using Bayesian capture–recapture models. We show that in populations with fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populations with slow life histories. Our study provides one of the few empirical examples of among‐population variation in actuarial senescence patterns in the wild and confirms that the fast–slow life‐history gradient is associated with both macroevolutionary and microevolutionary patterns of actuarial senescence. This paper is one of the few showing that position along the fast‐slow continuum predicts actuarial senescence patterns at the intraspecific level.

Evidence for actuarial senescence (i.e. the decrease in survival with increasing age) is now widespread across the tree of life. However, demographic senescence patterns are highly variable both between and within species. To understand these variations, there is an urgent need to go beyond aggregated mortality rates and to investigate how age‐specific causes of mortality in animals interact with age‐specific physiological performance. We address this question in the context of cancers. Cancer is a leading cause of death in human populations and has recently been shown to be more prevalent across species than previously thought. Since anthropogenic perturbations drastically increase cancer rates in wild populations of animals, deciphering the complex interactions between senescence and cancer now constitutes a key challenge in evolutionary ecology. Based on classical evolutionary theories of ageing, we first demonstrate that the occurrence of cancers might constitute an underestimated piece of the life‐history jigsaw. We propose that the selection for an increased allocation of resources towards growth and reproduction during early life might potentially favour cancer development, a life‐history pathway that might be functionally mediated by the process of immunosenescence. While we discuss the relevance of other proximate mechanisms suggesting that cancer arises as a direct consequence of senescence, we also argue that cancer itself can promote senescence by notably increasing the amount of resources required for somatic maintenance. Contrary to theoretical predictions, recent empirical evidence suggests that senescence is an asynchronous process among physiological functions. At the same time, the timing of occurrence varies widely between the different types of cancers. We suggest that similar evolutionary forces might shape the synchronicity of senescence and cancer patterns, which emphasize the tight and complex relationships linking these processes. We propose a conceptual background to lay down the foundations and the directions of future research projects aiming to disentangle the dynamic relationship between the evolution of cancer and senescence. We argue that studies embracing these research directions will markedly improve our understanding of both cancer prevalence and timing at the individual, population and species level. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.

Why and how we age are 2 intertwined questions that have fascinated scientists for many decades. However, attempts to answer these questions remain compartmentalized, preventing a comprehensive understanding of the aging process. We argue that the current lack of knowledge about the evolution of aging mechanisms is due to a lack of clarity regarding evolutionary theories of aging that explicitly involve physiological processes: the disposable soma theory (DST) and the developmental theory of aging (DTA). In this Essay, we propose a new hierarchical model linking genes to vital rates, enabling us to critically reevaluate the DST and DTA in terms of their relationship to evolutionary genetic theories of aging (mutation accumulation (MA) and antagonistic pleiotropy (AP)). We also demonstrate how these 2 theories can be incorporated in a unified hierarchical framework. The new framework will help to generate testable hypotheses of how the hallmarks of aging are shaped by natural selection.

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 tradeoffs, 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.

In most mammals, both sexes display different survial patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

Trade-offs between life history traits are expected to occur due to the limited amount of resources that organisms can obtain and share among biological functions, but are of least concern for selection responses in nutrient-rich or benign environments. In domestic animals, selection limits have not yet been reached despite strong selection for higher meat, milk or egg yields. Yet, negative genetic correlations between productivity traits and health or fertility traits have often been reported, supporting the view that trade-offs do occur in the context of nonlimiting resources. The importance of allocation mechanisms in limiting genetic changes can thus be questioned when animals are mostly constrained by their time to acquire and process energy rather than by feed availability. Selection for high productivity traits early in life should promote a fast metabolism with less energy allocated to self-maintenance (contributing to soma preservation and repair). Consequently, the capacity to breed shortly after an intensive period of production or to remain healthy should be compromised. We assessed those predictions in mammalian and avian livestock and related laboratory model species. First, we surveyed studies that compared energy allocation to maintenance between breeds or lines of contrasting productivity but found little support for the occurrence of an energy allocation trade-off. Second, selection experiments for lower feed intake per unit of product (i.e. higher feed efficiency) generally resulted in reduced allocation to maintenance, but this did not entail fitness costs in terms of survival or future reproduction. These findings indicate that the consequences of a particular selection in domestic animals are much more difficult to predict than one could anticipate from the energy allocation framework alone. Future developments to predict the contribution of time constraints and trade-offs to selection limits will be insightful to breed livestock in increasingly challenging environments.