Evolution of Aging Age is a very high price to pay for maturity (Tom Stoppard) Prospero in The Tempest says “We are such stuff as dreams are made on, and.

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Presentation transcript:

Evolution of Aging Age is a very high price to pay for maturity (Tom Stoppard) Prospero in The Tempest says “We are such stuff as dreams are made on, and our little life is rounded with a sleep.” How did Mark Twain put it? “I was dead for millions of years before I was born and it never inconvenienced me a bit.”

I. Evidence for senescence and evidence for the evolution of senescence Figure 13.4 Aging in three animals (a) Aging in a bird. For females in a wild population of collared flycatchers (Ficedula albicollis), the number of young fledged each year declines after age 3 (age-related differences in number fledged are significant at P < 0.001). The probability of survival from one year to the next declines slightly, but not significantly, after age 2. Sample sizes in parentheses. From Gustafsson and Part (1990). (b) Aging in a mammal. For males in a wild population of red deer (Cervus elaphus), the number of calves fathered each year declines sharply after a peak at about age nine; for females, the number of calves produced each year declines gradually starting at about age 13. For both sexes, the probability of surviving from one year to the next is nearly 100% from age 2 to 9. After age 9, the probability of surviving plummets. From Clutton-Brock et al. (1988). (c) Aging in an insect. For females in a laboratory population of fruit flies (Drosophila melanogaster), the average number of eggs laid per day declines after the age of about 12 days. In three laboratory populations, the probability of surviving from one day to the next falls at the age of about 20 days. Modified from Rose (1984).

Artificial selection increases life span in fruit flies Inherent limits, or can lifespan evolve? Fruit fly expt: Figure 13.6 Artificial selection increases life span in fruit flies The graph shows average life span in each of four laboratory populations of Drosophila melanogaster over 13 generations of selection. The vertical lines show the 95% confidence intervals for the estimated population averages. From Luckinbill et al. (1984).

II. Fundamental Trade-offs Female sockeye salmon defending its nest before dying

Mite Kiwi bird Figure 13.1a Extreme reproductive strategies (a) Having devoured their mother from the inside, three thrips egg mites (Adactylidium sp.) prepare to depart her empty cuticle. The mother's legs are visible at lower right (180x). Reproduced by permission from Elbadry and Tawfik (1966). Mite Kiwi bird

Figure 13.3 Short-winged and long-winged morphs of female sand crickets (Gryllus firmus)

The life history of a hypothetical female Virginia opossum (Didelphis virginiana) Figure 13.2 The life history of a hypothetical female Virginia opossum (Didelphis virginiana) This hypothetical female has a life history typical of female Virginia opossums living in the mainland United States (Austad 1988; 1993). Figure designed after Charnov and Berrigan (1993).

III. Evolutionary theories of aging Background: Figure 13.10a A simple genetic model reveals two mechanisms through which aging can evolve (a) The life history of individuals with the wild-type genotype. The sum of the values in column 4 gives the expected lifetime reproductive success of wild-type individuals: 2.419. Expected Reproductive Success (RS) = Prob(Surviving) x #(Offspring)

Figure 13.10b A simple genetic model reveals two mechanisms through which aging can evolve (b) The life history of individuals with a mutation that causes death at age 14. The expected lifetime reproductive success of individuals with this mutation is 2.340. The mutation is deleterious, but not extremely so. Versus 2.419

Figure 13.10c A simple genetic model reveals two mechanisms through which aging can evolve (c) The life history of individuals with a mutation that causes maturation at age 2 and death at age 10. The expected lifetime reproductive success of individuals with this mutation is 2.663. The mutation is advantageous. See text for more details. Versus 2.419

Senescence reflects relaxed selection (drift) Two Theories Senescence reflects relaxed selection (drift) increased expression of deleterious recessive alleles increased genetic variation later in life B. Senescence reflects tradeoffs loci involved in senescence have early fitness effects balancing selection signature Not mutually exclusive

Mutation Accumulation Hypothesis (drift, non selection) Mutations expressed later in life, near the end of reproduction are effectively neutral Figure 13.11 An increase in inbreeding depression with age consistent with the mutation accumulation hypothesis of senescence If inbreeding depression is caused by recessive deleterious alleles and if natural selection acts more weakly against late-acting deleterious alleles, then inbreeding depression should increase with age. This graph, tracking inbreeding depression as a function of age in laboratory fruit flies, shows that it does. Drawn from data in Hughes et al. (2002).

B. Antagonistic Pleiotropy Hypothesis The longevity allele hx546 under (a) benign and (b) stressful conditions Figure 13.13 Under semi-natural conditions, the age-1 gene in the nematode worm C. elegans exhibits antagonistic pleiotropy This graph tracks the frequency of the hx546 allele of the age-1 gene, which causes increased longevity, in six experimental populations reared in the lab with ample food. The frequency of hx546 changed little over 10 generations, regardless of its starting frequency, indicating that the allele was effectively neutral. (b) This graph tracks the frequency of the hx546 allele in five populations reared under semi-natural conditions characterized by periodic bouts of starvation. The frequency of hx546 declined rapidly over 12 generations in all five populations, indicating that the allele was strongly selected against. From Walker et al. (2000). But little evidence that candidate gene approach explains variation in natural populations

Trade offs in fruit flies between longevity and reproduction Figure 13.14 The methuselah gene controls a trade-off between reproductive success versus longevity and stress resistance Normal female fruit flies die younger than homozygous methuselah mutants (a), but they have considerably higher lifetime reproductive success (b). These patterns, detected at 29 degrees C, change at other temperatures. Redrawn from Mockett and Sohal (2006). At least one gene for which mutations strongly affect lifespan in D. melanogaster (Methuselah or Mth) also exhibits extensive natural polymorphism, a natural cline in allele frequencies that parallels a cline in lifespan, and a molecular signature of selection (Schmidt et al. 2000). Mutant analysis can therefore potentially reveal genes contributing to natural variation. Such genes can then be subjected to functional and evolutionary analyses that test model predictions. This path is not easy, however. Although the effects of Mth on lifespan have been recognized for more than a decade (Lin et al. 1998), natural allelic variation at this gene has still not been directly implicated in the clinal variation in lifespan (Paaby & Schmidt 2008). Of the many candidate genes nominated by mutagenic or transgenic manipulation, Mth is the only one that has been formally associated with natural variation in lifespan or ageing. More generally, loci contributing to natural variation in traits such as lifespan, starvation resistance and male mating behaviour show little overlap with those known to have large effects on the same phenotypes when mutated (Mackay et al. 2009). These results suggest that the candidate-gene approach is not an efficient one for documenting the genetic basis of natural variation in senescence. 4.

Collared flycatchers: (a) natural variation and (b) experimental manipulations Extra eggs Figure 13.15 In collared flycatchers (Ficedula albicollis), natural variation and experimental manipulations demonstrate a trade-off between reproduction early in life versus reproduction late in life (a) Females that first breed at age 1 (blue boxes) have smaller clutches at ages 2, 3, and 4 than females that do not breed until age 2 (red boxes). The error bars indicate the standard errors of the estimated mean clutch sizes; the numbers above the symbols give the sample sizes. (b) Females given extra eggs at age 1 (red boxes) have progressively smaller clutches each year at ages 2, 3, and 4. In contrast, control females (blue boxes) do not begin to show a decline in clutch size until age 4. Note that the vertical scales are different. From Gustafsson and Pärt (1990).

Table 13.1 Reproductive allocation in annual versus perennial plants

Figure 13.16 A Virginia opossum and her young Opossums, like other marsupials, have relatively short life spans for mammals. But opossums in some populations have shorter life spans than opossums in others. This suggests that rates of aging evolve in nature.

Differences in mortality Differences maternal ability Figure 13.17 Female opossums on Sapelo Island age more slowly than female opossums on the mainland (a) The rate of survival from one month to the next falls more rapidly with age for mainland opossums than for island opossums. (b) Each graph shows total litter mass as a function of litter age for females in their first year of reproduction (green or red) and for females in their second year of reproduction (blue or yellow). In mainland females (top graph), offspring in second-year litters grow more slowly than offspring in first-year litters (P < 0.001). In island females, second-year litters grow just as fast as first-year litters. (c) Tail collagen fiber-breaking time increases more slowly with age in island females than in mainland females (P < 0.001). From Austad (1993). Physiological deterioration

IV. Evolution of Senescence and Human Reproduction Figure 13.18a Data on menopause (a) Reproductive senescence in women and men. These data are from the Ache, hunter-gatherers of Paraguay. The graph shows the probability that women and men will have a child born during the year that they are any given age. From Hill and Hurtado (1996).

from Ache hunger-gathers of Paraguay Functional capacity of various physiological systems in women as a function of age from Ache hunger-gathers of Paraguay Figure 13.18b Data on menopause (b) This graph shows the functional capacity of various physiological systems in women as a function of age. Capacity is calculated as the fraction of youthful capacity still remaining. From Hill and Hurtado (1991); see citations therein for sources of data.

Menopause an artifact of living longer?? Probably NOT Figure 13.18d Data on menopause (d) Fraction of individuals surviving as a function of age in three hunter-gatherer cultures. From Hill and Hurtado (1991); see citations therein for sources of data.

Figure 13.18e Data on menopause (e) Time spent foraging each day during the wet season (left) and the dry season (right) by Hadza women of different ages: I = women who have reached puberty, but not yet married or begun to have children; II = women who are pregnant or have young children; III = women who are past childbearing age and have no children younger than 15. Blue circles represent women nursing young children. From Hawkes et al. (1989).

Hazda Woman (hunter-gatherer from East Africa) Figure 13.18f Data on menopause (f) This Hadza woman is approximately 65 years old. She is using a digging stick and muscle power to dig tubers from underneath large rocks. Digging tubers requires knowledge, skill, patience, strength, and experience, making Hadza grandmothers the most productive foragers.

Conclusion All organisms die The timing of reproduction and death can evolve Two evolutionary theories of senescence: Mutation Accumulation & Antagonistic Pleiotropy Human Menopause may be explained by inclusive fitness

Adult house flies only allowed to live 4 days Figure 13.12 Evolution of shorter life spans consistent with the accumulation of deleterious mutations In populations of individuals allowed to live only a short time, late-acting mutations are effectively neutral. Some of these alleles will rise to high frequency by drift, causing a decline in natural longevity. Such a decline is evident in this graph, which tracks the natural longevity over 24 generations in populations of houseflies in which the adults were allowed to live only four days. Redrawn from Reed and Bryant (2000). See box 7.5