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.

Figure 1

The evidence in support of senescence occurring in wild animals is now overwhelming. The plots use the studies listed in Table S1 to illustrate the rapidly accumulating number of: (A) new species in which age-related changes consistent with senescence have been documented in the wild and, (B) individual studies documenting or investigating senescence patterns in wild populations. The data is split to separately illustrate the evidence for birds, mammals, other vertebrates (fish, reptiles and amphibians), and invertebrates. (C) shows the cumulative number of studies documenting age-related change in survival probability, reproductive performance traits and change in other, typically physiological, traits with age indicative of senescence. Note that many studies document senescence in more than one type of trait, and that in all plots the first year (1976) on the graphs included the handful of studies up to and including that year.

Figure 2

The total number of new species per year (blue circles) and total number of studies per year (red triangles) documenting senescence in wild animal populations (from Table S1), with quadratic regression lines plotted through the points. There has been an accelerating increase in the number of new studies per year over the last decade, reflecting a shift towards in-depth research programs into aging patterns on single high-quality long-term study systems in the wild.