Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

Abstract

That senescence is rarely, if ever, observed in natural populations is an oft-quoted fallacy within bio-gerontology. We identify the roots of this fallacy in the otherwise seminal works of Medawar and Comfort, and explain that under antagonistic pleiotropy or disposable soma explanations for the evolution of senescence there is no reason why senescence cannot evolve to be manifest within the life expectancies of wild organisms. The recent emergence of long-term field studies presents irrefutable evidence that senescence is commonly detected in nature. We found such evidence in 175 different animal species from 340 separate studies. Although the bulk of this evidence comes from birds and mammals, we also found evidence for senescence in other vertebrates and insects. We describe how high-quality longitudinal field data allow us to test evolutionary explanations for differences in senescence between the sexes and among traits and individuals. Recent studies indicate that genes, prior environment and investment in growth and reproduction influence aging rates in the wild. We argue that – with the fallacy that wild animals do not senesce finally dead and buried – collaborations between bio-gerontologists and field biologists can begin to test the ecological generality of purportedly ‘public’ mechanisms regulating aging in laboratory models.

Senescence rates and late adulthood reproductive success are strongly influenced by personality in a long-lived seabird

“…It is widely thought that senescence may occur as a result of an accumulation of cellular damage caused during the lifetime of an individual, such that there is conflict between investment in current reproduction and investment in repair of organismal damage when resources are limited [4,5]. There is increasing empirical evidence that individuals differ in their rate of senescence, and this suggests individual level trade-offs between current and future reproduction [1,[6][7][8], but what leads individuals to engage in different life-history tactics is poorly understood.…”

“…In the last decade, there has been a surge in studies highlighting senescence in wild populations [1,2]. These reductions in reproductive performance or survival probability at old ages have deleterious effects on individual fitness [3].…”

Effects of the level of early productivity on the lifespan of ewes in contrasting flock environments

“…With regard to high prolificacy ewes, our results indicate that their survival at 4 years old and more can be impaired by a temporary underfeeding during early productive life. Such a phenomenon is widely shown in the wild (Nussey et al, 2013) and is generally explained by an accelerated deterioration of the reproductive or survival functions, or both, with age for animals that grew quickly and reproduced precociously (Lemaître et al, 2015). Although domesticated sheep breeds may show an earlier loss of the reproductive function than wild breeds (Mysterud et al, 2002), the present analysis of marginal stayability (4|3 and 5|4) suggests that the negative effects of NLB 2-3 on ewes' lifespans occurred shortly after the early reproductive effort, probably before the onset of reproductive senescence.…”

Effect of lifespan and age on reproductive performance of the tardigrade Acutuncus antarcticus: minimal reproductive senescence

“…Senescence is well documented in a variety of animals including wild populations of birds and mammals (Nussey et al, 2013). Among invertebrate species, the ageing process Correlations of each reproductive trait of individuals with lifespan and traits of overall oviposition events with clutch size were analysed using Kendall's tau statistic a Data reported in Tsujimoto et al (2015) b Data from individuals undergoing more than three oviposition events were included in these analysis in order to obtain reasonable estimation of the average c Data from clutches from the second oviposition event onwards were analysed.…”