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Journal ArticleDOI

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

TL;DR: It is argued 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.
About: This article is published in Ageing Research Reviews.The article was published on 2013-01-01 and is currently open access. It has received 529 citations till now. The article focuses on the topics: Senescence.

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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Citations
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TL;DR: This review summarizes the current knowledge regarding the formation of mtDNA mutations and their impact on mitochondrial function and critically discusses proposed pathways interlinked with mammalian mt DNA mutations and suggest future research strategies to elucidate the role of mitochondrial mutations in aging.

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Cites background from "Senescence in natural populations o..."

  • ...Although often mistaken to exist only among modern humans and animals in captivity, in reality most, if not all, metazoans show some signs of aging during their lifetime (Nussey et al., 2013)....

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Journal ArticleDOI
TL;DR: A review of 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life.
Abstract: 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 trade-offs, 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.

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BookDOI
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TL;DR: This chapter provides a general historical background, with definitions and information of free radicals, antioxidants and oxidative stress and examines how mild doses of stress can have stimulatory effects on organismal performance through hormetic mechanisms and that this may significantly relate to evolutionary fitness and to the ecology of species.
Abstract: The transition from a reducing to an oxidising chemistry in the atmosphere and oceans paved the way for the diversification of life. Oxygen expanded metabolic and biochemical capacities of organisms. Over the incipient stages of evolution of oxidative metabolism, organisms also needed to develop mechanisms to mitigate the toxic effects of oxygen derivatives, such as free radicals and nonradical reactive species. This chapter provides a general historical background, with definitions and information of free radicals, antioxidants and oxidative stress. This chapter also examines how mild doses of stress can have stimulatory effects on organismal performance through hormetic mechanisms and that this may significantly relate to evolutionary fitness and to the ecology of species. Finally, the chapter explains the concept of life-history trade-offs and highlights how the need to manage oxidative stress in an optimal way may be an important mechanism driving the outcome of many of these trade-offs. 1.1 The Great Oxidation Event: From a Reducing to an Oxidising World The planet Earth is approximately 4.5 billion years old. The atmosphere of the primeval Earth was quite different from what we observe nowadays. It was mildly reducing, with large proportions of methane, ammonia and hydrogen and a low concentration of oxygen (Schopf and Klein 1992; Sessions et al. 2009). Around 2.45 billion years ago, atmospheric oxygen rose suddenly in what is now termed the Great Oxidation Event (Sessions et al. 2009). A second significant increase in atmospheric oxygen occurred at around 600–800 million years ago and was accompanied by the oxygenation of the deep oceans and emergence of multicellular animals (Sessions et al. 2009). The increase in oxygen concentration in the atmosphere and oceans paved the way for the diversification of life (Fig. 1.1). D. Costantini, Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology, DOI: 10.1007/978-3-642-54663-1_1, Springer-Verlag Berlin Heidelberg 2014 1 The transition from a reducing to an oxidising atmosphere was characterised by the evolution of metabolic networks of increasing complexity (Raymond and Segrè 2006). Adaptation to molecular oxygen has also likely taken place independently in species from diverse lineages, even if it is unclear whether it contributed to shaping taxonomical diversity (Raymond and Segrè 2006). Certainly, oxygen expanded metabolic and biochemical capacities of organisms. The stimulatory effect of oxygen on the evolution of metabolic networks was not cost-free. Beyond diversification of mechanisms using oxygen to produce energy, organisms also needed to evolve mechanisms to mitigate the toxic effects of oxygen derivatives, such as free radicals and non-radical reactive species. 1.2 Reactive Species, Antioxidants and Oxidative Stress 1.2.1 On the Nature of Free Radicals and Other Reactive Species The discovery of organic free radicals dates back to over a century ago, when the scientist Gomberg (1900) at the University of Michigan identified the triphenylmethyl The primeval Earth’s atmosphere was mildly reducing. Photochemical reactions between simple gas elements 2H2 + CO2 → H2CO + H2O Evolution of anaerobic bacteria H2S + CO2 → (H2CO)n + S Evolution of photosynthetic organisms H2O + CO2 → (H2CO)n + O2 Evolution of aerobic eukaryotes; aerobic pathways produce much more energy than anaerobic pathways O2 + (H2CO)n → H2O + CO2 Aerobic pathways generate oxygen free radicals and non-radical species. Hence, evolution of antioxidant mechanisms to cope with oxidative stress. Fig. 1.1 Sequence of main transitions in energetic metabolism induced by changes in atmosphere and ocean chemistry (see Falkowski 2006) 2 1 Historical and Contemporary Issues of Oxidative Stress

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TL;DR: Major insights and challenges that have emerged over the last 35 years are reviewed: selection does not always necessarily decline with age; higher extrinsic mortality does notalways accelerate aging; conserved pathways control aging rate; senescence patterns are more diverse than previously thought and aging is not universal.
Abstract: Between the 1930s and 50s, evolutionary biologists developed a successful theory of why organisms age, firmly rooted in population genetic principles. By the 1980s the evolution of aging had a secure experimental basis. Since the force of selection declines with age, aging evolves due to mutation accumulation or a benefit to fitness early in life. Here we review major insights and challenges that have emerged over the last 35 years: selection does not always necessarily decline with age; higher extrinsic (i.e., environmentally caused) mortality does not always accelerate aging; conserved pathways control aging rate; senescence patterns are more diverse than previously thought; aging is not universal; trade-offs involving lifespan can be ‘broken’; aging might be ‘druggable’; and human life expectancy continues to rise but compressing late-life morbidity remains a pressing challenge.

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TL;DR: The Biology of SenescenceBy Dr. Alex Comfort.
Abstract: The Biology of Senescence By Dr Alex Comfort Pp xiii + 257 (London: Routledge and Kegan Paul, Ltd, 1956) 25s net

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References
More filters
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TL;DR: August Weismann's theory is subject to a number of criticisms, the most forceful of which are: 1) The fallacy of identifying senescence with mechanical wear, 2) the extreme rarity, in natural populations, of individuals that would be old enough to die of the postulated death-mechanism, 3) the failure of several decades of gerontological research to uncover any deathmechanisms, and 4) the difficulties involved in visualizing how such a feature could be produced
Abstract: A new individual entering a population may be said to have a reproductive probability distribution. The reproductive probability is zero from zygote to reproductive maturity. Later, perhaps shortly...

3,981 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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  • ...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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TL;DR: A new individual entering a population may be said to have a reproductive probability distribution as discussed by the authors, where the reproductive probability is zero from zygote to reproductive maturity, i.e., the individual will have no reproductive capability from birth to maturity.
Abstract: A new individual entering a population may be said to have a reproductive probability distribution. The reproductive probability is zero from zygote to reproductive maturity. Later, perhaps shortly...

3,800 citations

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16 Apr 2010-Science
TL;DR: Dietary restriction and reduced activity of nutrient-sensing pathways may slow aging by similar mechanisms, which have been conserved during evolution, and their potential application to prevention of age-related disease and promotion of healthy aging in humans, and the challenge of possible negative side effects.
Abstract: When the food intake of organisms such as yeast and rodents is reduced (dietary restriction), they live longer than organisms fed a normal diet. A similar effect is seen when the activity of nutrient-sensing pathways is reduced by mutations or chemical inhibitors. In rodents, both dietary restriction and decreased nutrient-sensing pathway activity can lower the incidence of age-related loss of function and disease, including tumors and neurodegeneration. Dietary restriction also increases life span and protects against diabetes, cancer, and cardiovascular disease in rhesus monkeys, and in humans it causes changes that protect against these age-related pathologies. Tumors and diabetes are also uncommon in humans with mutations in the growth hormone receptor, and natural genetic variants in nutrient-sensing pathways are associated with increased human life span. Dietary restriction and reduced activity of nutrient-sensing pathways may thus slow aging by similar mechanisms, which have been conserved during evolution. We discuss these findings and their potential application to prevention of age-related disease and promotion of healthy aging in humans, and the challenge of possible negative side effects.

2,522 citations


"Senescence in natural populations o..." refers background in this paper

  • ...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)....

    [...]

  • ...…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)....

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  • ...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)....

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Journal ArticleDOI
TL;DR: A basis for the theory that senescence is an inevitable outcome of evolution is established and the model shows that higher fertility will be a primary factor leading to the evolution of higher rates ofsenescence unless the resulting extra mortality is confined to the immature period.

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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Journal ArticleDOI
09 Nov 2000-Nature
TL;DR: The evolutionary theory of ageing explains why ageing occurs and helps to clarify how the genome shapes the ageing process, thereby aiding the study of the genetic factors that influence longevity and age-associated diseases.
Abstract: The evolutionary theory of ageing explains why ageing occurs, giving valuable insight into the mechanisms underlying the complex cellular and molecular changes that contribute to senescence. Such understanding also helps to clarify how the genome shapes the ageing process, thereby aiding the study of the genetic factors that influence longevity and age-associated diseases.

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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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