The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

Abstract

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.

Sex‐independent senescence in a cooperatively breeding mammal

“…From such work, it has become increasingly clear that different fitness‐related traits can display divergent age‐related trajectories within individuals (Evans, Gustafsson, & Sheldon, ; Hayward et al, ; Nussey et al, ), and are not necessarily closely related to each other (Bouwhuis, Choquet, Sheldon, & Verhulst, ). These observations contradict Williams’ prediction that senescence ‘should always be a generalized deterioration’ (1957; see Gaillard & Lemaître, ) and highlight the need to consider a wider range of life histories to better understand the operation of senescence in natural populations.…”

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

“…Since Williams’ () pioneering contribution on this topic, the relationship between environmentally driven mortality and actuarial senescence has been heavily discussed (see Gaillard & Lemaître, and Ronget, Garratt, Lemaître, & Gaillard, for reviews). According to Williams (), high level of adult mortality should lead to a much stronger rate of actuarial senescence, a prediction which was validated by simulations (Gaillard & Lemaître, ), at least in the absence of density‐dependent or condition‐dependent mortality over the entire life course (Abrams, , Williams & Day, ; see also Moorad, Promislow, & Silvertown, for a recent review). For instance, if mortality during the juvenile period is strongly condition‐dependent, only the most robust individuals will reach adulthood which can postpone and/or decrease actuarial senescence rates (Ronget et al, ).…”

“…survival) at advanced ages. So far, most studies focused on ageing in the wild have been embedded within the two theoretical frameworks offered by both antagonistic pleiotropy and disposable soma theories of ageing as these two theories share the similar prediction of a trade‐off between reproductive effort and actuarial senescence (Gaillard & Lemaître, ).…”

Are trade‐offs really the key drivers of ageing and life span?

“…These hypotheses have been recently discussed in the light of new empirical evidence (reviewed in Gaillard & Lemaître, 2017) demonstrating that demographic, phenotypic and functional senescence are not synchronous (e.g. in Soay sheep in Hayward et al (2015) or in BOX 1 Trade-off between mortality components may explain non-synchronicity of senescence by causes of deaths Let us assume a theoretical organism, absent of extrinsic mortality, whose adult mortality hazard (t) is shaped by three independent additive Gompertz-shaped (i.e.…”