Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology
Summary (3 min read)
1.2. Unravelling the fallacy
- Current empirical support from model laboratory organisms for disposable soma theory and antagonistic pleiotropy as mechanisms of senescence is dramatically stronger than for mutation accumulation.
- Many single gene mutations known to extend life in model laboratory organisms have detrimental effects on early components of Darwinian fitness (Table 1 ).
- If antagonistic pleiotropy and disposable soma are the main mechanisms responsible for the evolution of senescence and the maintenance of genetic variation in aging and lifespan, the authors should expect to observe senescence in the wild.
2. Senescence in wild animals -an evidentiary review
- Of these, the vast majority were birds and mammals -149 studies of 75 bird species and 165 studies of 79 mammal species.
- Table 2 spreads the evidence for senescence in the wild (Table S1 ) across the orders of birds and placental mammals.
- This serves to illustrate that the evidence is reasonably well taxonomically spread.
- Indeed, their survey of the literature suggests to us that where senescence has been looked for with detailed longitudinal data in wild birds and mammals it is usually found.
- Table 2 also clearly shows that there are many, many orders and genera for which data are.
Table 2
- Phylogenetic distribution of studies documenting evidence of senescence in wild populations of birds and placental mammals.
- Note that an absence of evidence for senescence within orders or genera most likely reflects ecological ignorance regarding the taxa in question, rather than evidence that senescence does not occur.
Birds
- It is very important to be aware that in Table 2 an absence of evidence for senescence reflects ecological ignorance regarding the taxa in question, rather than evidence that senescence does not occur.
- Monitoring fecundity and reproductive performance in the wild is exceptionally challenging in reptiles (not to mention fish or amphibians), and many studies have circumvented this by bringing wild-caught females into the laboratory to breed and subsequently releasing them and their young back at their original capture site (e.g. Massot et al., 2011; Sparkman et al., 2007) .
- The data are split to separately illustrate the evidence for birds, mammals, other vertebrates (fish, reptiles and amphibians), and invertebrates.
- Research into senescence and lifespan in wild insects is an exciting area with unique potential to link their understanding of aging in laboratory conditions to aging in a realistic evolutionary context (Carey, 2011; Zajitschek et al., 2009b) .
- Although some meticulous analyses of high quality data from wild bird and mammal populations have failed to find evidence of senescence (e.g.
3. Understanding the causes and consequences of variation in senescence in wild animal populations
- Longitudinal studies in natural populations can also provide crucial insight into the drivers of individual variation in senescence, and in the last decade, there has been growing interest and activity among researchers studying wild animals towards this aim.
- Fig. 2 shows that the increase through time in the number of studies investigating senescence in the wild has been considerably more rapid than the increase in number of new species in which senescence has been documented in nature, over the last 15 years or so.
- Below the authors review progress in addressing several questions of considerable interest to bio-gerontologists in wild animal populations.
- 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.
3.1. Sex differences in senescence
- Long-term individual-based field studies often collect longitudinal data on a host of phenotypic traits, including behavioural, reproductive and physiological parameters, as well as information on survival, as already discussed (see Section 3).
- There is also some evidence from wild female ungulates that fecundity senescence may begin later and progress more rapidly than age-related declines in survival probability (Bérubé et al., 1999; Catchpole et al., 2004; Jorgenson et al., 1997; Nussey et al., 2009) .
- Emerging data suggest that male secondary sexual traits -despite theoretical expectations that they should be physiologically costly (Andersson, 1994) -do not actually senesce, although reproductive performance clearly does (Evans et al., 2011; Nussey et al., 2009) .
3.3. Individual, genetic and environmental variation in senescence rates
- Studies in wild animals provide spectacular examples of the effect that the environment can have on the aging process.
- A comparison of mortality curves in wild and laboratory stalked-legged flies revealed that males senesce at least twice as rapidly under natural conditions as in the laboratory (Kawasaki et al., 2008) .
- An interesting pattern emerged from a recent study of tawny owls, which experience profound variation in food availability associated with population cycles of their main prey.
- Field researchers, particularly those working on birds, have a long history of integrating longitudinal field data collection with experimental manipulation.
3.4. Tests of life history theories of aging
- A long-term study of collared flycatchers in Sweden, where researchers experimentally increased the brood size of females in early adulthood, has shown that these females produced consistently smaller subsequent broods, with a suggestion that brood size also declined more rapidly with age, compared to control females (Gustafsson and Part, 1990) .
- Subsequently, studies of female great tits, guillemots and red deer have all demonstrated that increases in fecundity or reproductive performance in early adulthood are associated with more rapid declines in reproductive performance in later life (Bouwhuis et al., 2010a; Nussey et al., 2006; Reed et al., 2008) .
- Also, mute swans that start their breeding careers earlier in life end their reproductive lifespan earlier as well (Charmantier et al., 2006b) , and red squirrels that start breeding early have shorter subsequent life expectancies (Descamps et al., 2006 ).
- Those that allocate relatively more in offspring at two years of age actually show increased subsequent reproductive success but at the cost of more rapid declines in survival probability, in essence sacrificing lifespan for high reproductive output (Massot et al., 2011) .
- Where field studies have tested the predictions of life history theories of aging with detailed longitudinal data and robust statistics, they have tended to find support (Peron et al., 2010) .
4. Conclusions: why bio-gerontologists should care about aging in natural populations
- To date, discourse between bio-gerontologists interested in identifying conserved mechanisms underpinning the aging process and evolutionary ecologists interested in explaining variation in the natural world using evolutionary theory has been limited.
- The authors argue this can and should change, and this would be to the mutual benefit of both sides.
- Furthermore, the increasing availability and affordability of next generation genomic tools in non-model systems means that field ecologists and bio-gerontologists could collaborate to test whether genes associated with aging and lifespan in humans and model organisms show any variation in wild populations, and determine how natural selection acts to maintain any evident genetic variation.
- Whilst evidence for such costs associated with dietary or physiological interventions that extend lifespan in model organisms are mounting (Table 1 ), these may only poorly reflect the actual costs of increasing life-or healthspan in more challenging environments.
- More generally, the detailed longitudinal data collected by field ecologists will allow researchers to link growth and development, parental care and infection in early life with health and survival in later adulthood in a manner rarely possible in either laboratory models or in extremely long-lived species like humans.
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References
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"Senescence in natural populations o..." refers background in this paper
...Classical evolutionary theory does not refer to or consider a state of senility in very late adulthood, rather it predicts that senescence should begin at the age of sexual maturity and progress from that point as the force of natural selection weakens (Hamilton, 1966; Williams, 1957)....
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...Evolutionary theory offers explanations for how and why differences in lifespan and aging might have arisen under natural selection (Bonduriansky et al., 2008; Williams, 1957)....
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...Based on the idea that the strength of natural selection against senescence hinges on the rate of ‘extrinsic mortality’ experienced in nature, Williams (1957) predicted “where there is a sex difference [in “extrinsic” mortality], the sex with the higher mortality rate and lesser rate of increase…...
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...– Williams, 1957 By way of example, Williams noted that an examination of athletic records reveals ‘rampant’ senescence in humans as early as their 30’s, a period which no-one could disagree humans commonly reached even in a state of nature (Williams, 1957)....
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...Variation in senescence among traits Williams (1957) predicted that senescence in different physiological systems associated with fitness should progress in synchrony, and reiterated the “expected evolution of synchrony” in a much later monograph on aging (Williams, 1999)....
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...This research suggests conserved or ‘public’ genetic and physiological pathways, which are modulated by diet, across distantly related taxa to modulate aging and lifespan (Fontana et al., 2010; Partridge, 2010)....
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...…hat extend life- and health-span in a handful of short-lived rganisms under laboratory conditions has revolutionized our nderstanding of the aging process and raised real hopes of develping medical interventions that extend healthy life in humans Fontana et al., 2010; Partridge, 2010)....
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...The identification of environmental and genetic manipulations that extend life- and health-span in a handful of short-lived organisms under laboratory conditions has revolutionized our understanding of the aging process and raised real hopes of developing medical interventions that extend healthy life in humans (Fontana et al., 2010; Partridge, 2010)....
[...]
...This research suggests conserved or ‘pubic’ genetic and physiological pathways, which are modulated by iet, across distantly related taxa to modulate aging and lifespan Fontana et al., 2010; Partridge, 2010)....
[...]
1,966 citations
"Senescence in natural populations o..." refers background in this paper
...Classical evolutionary theory does not refer to or consider a state of senility in very late adulthood, rather it predicts that senescence should begin at the age of sexual maturity and progress from that point as the force of natural selection weakens (Hamilton, 1966; Williams, 1957)....
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"Senescence in natural populations o..." refers methods in this paper
...As already discussed, work on laboratory model systems generally supports these ‘life history’ theories of aging (Table 1, Kirkwood and Austad, 2000; Partridge and Barton, 1996)....
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