Aging and Other Life History Characters

1. Aging and Other Life History Characters Chapter 12

2. What is life history? • Life histories describe: • Age at maturity (age of 1st reproduction) (early or late) • Reproductive patterns (reproduce once or many times) • Number of offspring (many or few) • Size of offspring (large or small) • Life span (short or long) • Life history is a description of the way in which organisms realize their fitness • “Life history components” are “fitness components”

3. Life histories and trade-offs • Because the amount of energy than an organism can harvest is finite, life histories inevitably involve trade-offs: • many small vs. few large offspring • rapid reproduction and shorter life span vs. slower reproduction and longer life span • Natural selection should attempt to adjust the allocation of energy between growth, metabolism, repair, and reproduction in such a way as to maximize total lifetime reproduction (= fitness)

4. The life history of a hypothetical female Virginia opossum (Austad 1988, 1993) (fig. 12.2)

5. Life history theory attempts to answer questions such as the following: • Why do we age (senesce)? • Why do some species reproduce only once while other reproduce repeatedly? • Why do some species have many small offspring while others have only a few relatively large ones? • Why do some take a long time to reach reproductive maturity, others only a short time?

6. Aging and life span:what is aging? • Mortality senescence Decrease in the probability of survival, per unit time, as age increases • Reproductive senescence Decrease in reproduction with increasing age

7. Survivorship Patterns px is the probability of surviving from age x to x+1

8. Survivorship Patterns px is the probability of surviving from age x to x+1

9. Survivorship Patterns px is the probability of surviving from age x to x+1

10. Mortality Patterns qx is the probability of dying in the age interval x to x+1 (= 1 - px)

11. Aging in collared flycatchers: natural population (Gustafsson & Part 1990) (Fig. 12.4 a)

12. Aging in red deer: natural population (Clutton-Brock et al. 1988) (Fig. 12.4 b)

13. Aging in D. melanogaster: laboratory population (Rose 1984) (Fig. 12.4 c)

14. Rate-of-living theory of aging:“live fast, die young” • Aging is caused by accumulation of irreparable damage to cells and tissues • Damage is caused by errors in replication, transcription and translation; and by toxic metabolic by-products (oxidative damage, etc.) • All organisms have been selected to resist and repair cell and tissue damage to the maximum extent physiologically possible. They lack the genetic variation that would enable them to evolve more effective repair mechanisms than they already have.

15. Predictions of the rate-of-living theory of aging • Because cell and tissue damage is caused in part by the by-products of metabolism, the aging rate should be correlated with the metabolic rate, or, equivalently, different species (within broad taxonomic groups) should have similar per gram total lifetime energy expenditures • Because organisms have been selected to resist and repair damage to the maximum extent possible, species should not be able to evolve longer life spans

16. The data suggest that prediction (1) is not upheld (Austad & Fischer 1991) (Fig. 12.5) Bats, in particular, live almost 3 times longer than other mammals of similar size and metabolic rate Marsupials have significantly lower metabolic rates than other mammals of the same size, but also have significantly shorter life spans

17. Experiments show that prediction (2) is not upheld (Luckinbill et al. 1984) (Fig. 12.6) Life span of D. melanogaster is easily increased by selection in the laboratory. This means that there is heritable genetic variation for life span.

18. The “telomere” theory of aging • Telomeres are tandemly repeated nucleotide sequences that are placed on the ends of eukaryotic chromosomes by the enzyme telomerase (TTAGGG in humans) • Telomeres are necessary because linear chromosomes shorten with each round of replication. Without them, chromosomes would erode away • Telomerase is not expressed in most somatic cells • This means that somatic cells can undergo a limited number of mitotic divisions • Under this theory, individuals age because they can no longer replace damaged and worn-out cells

19. A prediction based on the “telomere” theory of aging • If life span is limited by the number of cell divisions, and different species have similar numbers of cell divisions before telomeres are eroded away, then the life spans of whole organisms should be correlated with the life spans of their constituent cells

20. Life span of cells and whole organisms (Rhome 1981) (Fig. 12.7)

21. The paradox of aging – 1 • The rate-of-aging and telomerase theories address the physiological, cellular and molecular causes of aging — whether correct or not, they leave an important question unanswered: • If laboratory fruit fly populations can evolve longer life spans, and bats have evolved longer life spans than other mammals of similar size and metabolic rate, and genetic engineers can increase the number of times cells can divide by artificially increasing telomerase expression, why has natural selection not produced longer life spans in all species?

22. The paradox of aging – 2 • All other things being equal, longer life span and high levels of reproduction into late age will equal greater fitness. Given that aging (senescence) reduces individual fitness and given that there is genetic variance for life span, why doesn’t natural selection reduce or eliminate aging? • To answer this question, we need an evolutionary theory of senescence

23. The evolutionary theory of senescence • Senescence occurs because the “force of selection” declines with advancing age. W. D. Hamilton 1966. The moulding of senescence by natural selection. J. Theoret. Biol. 12:12-45

24. A verbal argument • Death before reproduction = zero fitness • Death after reproduction begins = greater than zero fitness • Therefore: natural selection will work most effectively against lethal mutations that kill before reproduction begins, but less effectively against lethals that act later in life. • If harmful genetic effects are expressed late enough in life, selection against them will be negligible because most individuals carrying the harmful alleles will already have died from other causes (predation, accident, etc.)

25. A hypothetical non-senescent life history (constant survivorship, constant reproduction for ages ≥ 3, all individuals die before age 16) (Fig. 12.9 a)

26. A hypothetical non-senescent life history (constant survivorship, constant reproduction for ages ≥ 3, all individuals die before age 14) (Fig. 12.9 b)

27. A hypothetical non-senescent life history (constant survivorship, constant reproduction for ages ≥ 2, all individuals die before age 10) (Fig. 12.9 c)

28. Evolutionary genetic mechanisms • Mutation accumulation Peter Medawar (1952) — senescence due to deleterious alleles with effects confined to late ages — senescence evolves because natural selection is powerless to prevent it • Antagonistic pleiotropy (trade-offs) George Williams (1957) — senescence due to alleles with beneficial effects early in life but deleterious pleiotropic effects late in life —senescence is selectively advantageous

29. An implication of the evolutionary analysis • The rate of senescence of an organism should evolve by natural selection in response to environmental changes that alter the schedule of survivorship and fecundity — e.g., if the environmental force of mortality declines so that survivorship to later ages is increased, then selection should favor reduced rates of senescence (and vice versa).

30. Experimental evolution of life span in D. melanogaster Wild population(S. Amherst, MA) Laboratory population(IV) (B. Charlesworth, 1975) B selection 5 replicate populations (B1 – B5) 2 -wk discrete generations O selection 5 replicate populations (O1 – O5) 10 – 12 wk discrete generations (M. Rose, 1984)

31. Evolution of life span in laboratory populations of D. melanogaster (Service, Michieli, and McGill. 1998. Evolution 52:1844-1850). “B” populations are maintained on a 2-wk generation time and “O” populations are maintined on 10 – 12 wk generation times, which selects for longer life span. The “b” parameter describes the rate of increase in mortality rate with age: higher values equal more rapid mortality senescence. One-way ANOVA (df = 1, 7) was used to test for differences between selection regimes. Life span: F = 207.36, P < 0.0001; b: F = 94.82, P < 0.0001; PopulationCohort Life span b size (days) Short-generation B1 231 26.3 0.280 B2 167 26.2 0.318 B3 231 22.4 0.309 B4 196 24.8 0.274 B5 235 27.4 0.243 B mean 25.4 0.285 Long-generation O2 263 53.6 0.072 O3 289 65.2 0.062 O4 409 60.9 0.101 O5 307 63.7 0.128 O mean 60.9 0.091

32. Mortality rate vs. age in fly populations that have evolved different life spans • “B” flies are selected on short generation times; “O” flies are selected on long generation times • (Service, Michieli, and McGill. 1998. Evolution 52:1844-1850)

33. Female egg laying vs. age in fly populations that have evolved different life spans - evidence for antagonistic pleiotropy between early age reproduction and life span • “B” flies (solid squares) are selected on short generation times; “O” flies (open squares) are selected on long generation times • (Service, Michieli, and McGill. 1998. Evolution 52:1844-1850)

34. Laboratory evolution of life span in D. melanogaster (Luckinbill et al. 1984) (Fig. 12.6)

35. Increase in inbreeding depression with age is consistent with the mutation accumulation mechanism of senescence (Hughes et al. 2002) (Fig. 12.10)

36. Decrease in life span in houseflies when adults live ≥ 4 days is consistent with mutation accumulation (Reed and Bryant 2000) (Fig. 12.11)

37. Antagonistic pleiotropy in the age-1 gene of C. elegans (Walker et al. 2000) (Fig. 12.12) • Frequency of life-extending hx546 allele with no food shortage • Frequency of hx546 allele when environment is degraded

38. A phenotypic trade-off between early age and later age reproduction in collared flycatchers (Gustafsson & Part 1990) (Fig. 12.13) • Females that reproduce at age 1, have fewer offspring later in life • Females given extra offspring to raise at age 1, lay fewer eggs in subsequent years

39. How many offspring should an individual produce in a given year? • Clutch size in birds and Lack’s hypothesis (David Lack 1947) • Clutch size should be such that it maximizes the number of surviving offspring

40. A mathematical treatment of Lack’s hypothesis (Fig. 12.16) • Given the relationship between clutch size and the probability of survival of individual offspring, the clutch size that maximizes the number of surviving offspring is 5

41. Most birds lay smaller clutches than predicted by Lack’s hypothesis Clutch size and number of young per clutch in great tits (Boyce and Perrins 1987) (Fig. 12.17)

42. Reasons why birds may not behave according to Lack’s hypothesis • Lack’s hypothesis assumes that there is no trade-off between reproduction in one year and the next • Lack’s hypothesis assumes that the only effect of clutch size on the offspring is through their survivorship Clutch size of mothers affects clutch size of daughters in collared flycatchers (Schluter & Gustafsson 1993) (Fig. 12.18)