Sci. Aging Knowl. Environ., 27 November 2002
Vol. 2002, Issue 47, p. pe19
[DOI: 10.1126/sageke.2002.47.pe19]

PERSPECTIVES

Biologists Finally Horn In on Senescence in the Wild

Christine C. Spencer, and Daniel E. L. Promislow

The authors are in the Genetics Department at the University of Georgia, Athens, GA, 30602-7223, USA. E-mail: spencer{at}uga.edu (C.C.S.)

http://sageke.sciencemag.org/cgi/content/full/sageke;2002/47/pe19

Key Words: antler fly • Protopiophila • life-span • reproduction • senescence • survival • wild populations

"The weight of evidence suggests that senescence in the wild is rare but not unknown . . . If our observation of animal life-cycles were confined to small birds and mammals in the wild, however, we should probably not recognize senescence as an entity except in ourselves."
- From The Biology of Senescence, by Alex Comfort Introduction

If you were to ask most biologists about moose antlers, they would undoubtedly tell you a story about male-male competition and sexual selection. A new study by Bonduriansky and Brassil (1) suggests that antlers might also help us unlock the mysteries of aging in a natural population . . . of insects.

For years, biologists were sure that senescence--the decline in function with age--did not occur in natural populations, as Comfort cautiously stated in his pivotal text (2). Senescence couldn't occur in the wild, the argument went, because no wild animal would live long enough to die a natural death. Instead, the ferocity of "nature red in tooth and claw" (3) meant that animals perished at a young age, because they did not beg enough for food as hatchlings, were devoured by predators, or died battling for territory or mates. Only very special circumstances would lead to older, less fit individuals in a population. Shelter, agriculture, stable diet, weapons against predators, and, later on, information and the cultural memory carried by older individuals are features that might have allowed humans to continue living after they stopped reproducing.

Senescence in Wild Bird Populations

In fact, when we peer into natural populations with the proper lens, senescence turns out to be quite common in the wild. In certain populations of wild animals, researchers have identified individuals that exhibit reduced reproductive capacity with age, reduced age-specific survival, or both, indicating that they are experiencing senescence. Some of the best experimental demonstrations come from the small birds that Comfort (2) assumed would not live long enough to senesce. For example, the ability to reproduce declines quite dramatically with age in the collared flycatcher, which weighs in at about 16 g, whereas survival is constant with age in this species, instead of showing an age-specific decline consistent with senescence (4). In the slightly larger Florida scrub jay (~80 g), a 25-year census of a sedentary breeding population found a clear age-related decline in survival rate (5). Although these studies detect senescence in different traits (survival versus reproduction), both species show a decline in fitness with age. Why one species shows evidence of senescence in reproduction and the other in survival is a question that future studies would do well to address.

Are There Experimental Systems to Study Aging in the Wild?

Long-term studies can provide wonderfully detailed information about natural populations such as the Florida scrub jays, but learning how senescence evolves and identifying the factors that influence this process require an experimental system. A tractable system should have the following properties: The species must be short-lived, reproduce rapidly, and live in a closed population, so that each individual can be monitored for its entire life-span. Until now, these requirements have meant focusing on lab-reared organisms. Under controlled laboratory conditions, extrinsic mortality factors such as predation, environmental stresses, and limited resources do not prematurely remove individuals from the population. Indeed, in the absence of these extrinsic forces, researchers see clear evidence of senescence. However, as we pointed out in a recent Perspective (see Spencer and Promislow Perspective), there are pitfalls to studying the process of aging in lab-adapted organisms (6).

Most biogerontologists would argue that the experimental benefits of working with lab-reared organisms far outweigh any problems that might arise as these animals adapt to the lab environment. Wild populations, most would argue, are too difficult to work with and are not likely to exhibit senescence in any case. But despite obvious challenges, we can gain important insights about the aging process from wild populations. For example, in the work on scrub jays, the researchers discovered that the population consisted of two distinct types of individuals. One group of healthy individuals began breeding at age two and showed low levels of mortality early in life, followed by a significant increase in mortality as they aged. The second group was made up of laggards who did not breed until age three and displayed poor fitness relatively early in life, and therefore had high enough early mortality to muddy the pattern of aging. These two groups represent two complementary life history strategies in a single population, each with its own pattern of aging. In this case, work on a natural population provides insight into the evolutionary forces that could maintain genetic variation for life-span within a single population.

Senescence in Antler Flies

What we really need is an organism with the benefits of fruit flies--small, short-lived, and easily manipulated--that can be studied in a natural environment. A new study by Bonduriansky and Brassil (1) suggests that the recently discovered antler fly (Protopiophila litigata) (Fig. 1), which has a mean life-span of just 7.5 days, might be exactly what researchers have sought. Protopiophila live out their lives on the discarded antlers of moose (Fig. 2). Once established on an antler, males stake out their little piece of territory on the antler's upper surface, so the population is easy to monitor. In spite of their high extrinsic mortality (13% per day, on average), Bonduriansky and Brassil (1) found that both survival and reproductive rates declined with age, indicating that senescence is occurring in this natural population. This result adds to mounting evidence that senescence can and does occur in the wild. Bonduriansky and Brassil's demonstration of senescence in antler flies "will, I hope, drive a wooden stake through the assumption that animals in nature never age," asserts Steven Austad, University of Idaho, who is noted for his own work on aging in natural populations of opossums.



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Fig. 1. Marked male P. litigata guarding his territory on a moose antler. [Credit: R. Bonduriansky/University of Toronto]

 


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Fig. 2. Population of P. litigata on the upper surface of a discarded moose antler. Bonduriansky and Brassil (1) drew a numbered grid on the antler to monitor the movement of individuals within the population. [Credit: R. Bonduriansky/University of Toronto]

 
Selection Pressures and Aging

Bonduransky and Brassil's study does more than close the door on doubts about the occurrence of senescence in wild populations. The antler fly study system provided a rare opportunity to examine the strength of selection on both declining survival and declining reproductive capacity. This exercise can give us some indication of how selection has acted on fitness traits in the past and how these traits are likely to evolve in the future.

The rationale and method for measuring the strength of selection on life history traits come from evolutionary theories of senescence (see "Aging Research Grows Up"). Two widely cited models, "mutation accumulation" (7) and "antagonistic pleiotropy" (Williams Classic Paper), rest on the following insight: A deleterious mutation that reduces survival or fecundity early in life will be removed by the force of natural selection. A gene with equivalent effects on survival or fecundity, but whose effects are confined to late ages, will experience little selection. Thus, late-acting deleterious mutations will accumulate over evolutionary time, and so lead to the age-related decline in fitness traits that we call senescence. This argument depends on the existence of a steady decline in the strength of selection with age. Hamilton (8) showed mathematically that this is indeed the case. Given rates of survival (px) and reproduction (mx) for each age, x, in a population, we can use fairly simply matrix models to determine the strength of selection acting on each trait at each age (8, 9). If the fitness of a population is given by its net per-capita growth rate, {lambda}, the strength of selection acting on p or m at some age is simply the sensitivity of {lambda} to small changes in that trait at a given age. Readily available software packages such as MATLAB or Mathematica allow one to calculate these sensitivities easily.

Bonduriansky and Brassil carried out this type of sensitivity analysis for their population of antler flies. They found that early in life, survival was under stronger selection than reproduction, but by about day 20, selection pressures shifted from survival to mating rate, a measure of reproductive effort. In addition, the overall fitness costs of reproductive senescence were almost twice that of the age-specific increase in mortality rate. Although this relationship was not significant, it implies that selection pressures that lead to senescence in these two traits differ in strength.

Conclusion

In the 7 years since Bonduriansky first described antler flies (10), he and his colleagues have documented the flies' mating system (11), observed positive assortative mating by body size, found evidence for male choosiness in mates (12), and determined that males battle one another for territories (13). In short, antler flies have a complex ecology and life history strategy. Now that we know they senesce, antler flies provide a unique opportunity to examine aging in the wild and to tease apart the relationship between aging and sexual selection. Thus, the moose antler could provide a much-needed natural observation post for studies on the short-lived antler fly and the evolution of aging.


November 27, 2002
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  2. A. Comfort, The Biology of Senescence (Elsevier North Holland, New York, 1956).
  3. A. Tennyson, In Memoriam (E. Moxon, London, ed. 2, 1850).
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  10. R. Bonduriansky, A new Nearctic species of Protopiophila Duda (Diptera: Piophilidae), with notes on its behaviour and comparison with P-latipes (Meigen). Can. Entomol. 127, 859-863 (1995).
  11. R. Bonduriansky, R. J. Brooks, Copulation and oviposition behaviour of Protopiophila litigata (Diptera:Piophilidae). Can. Entomol. 130, 399-405 (1998).
  12. R. Bonduriansky, R. J. Brooks, Male antler flies (Protopiophila litigata; Diptera:Piophilidae) are more selective than females in mate choice. Can. J. Zool. 76, 1277-1285 (1998).[CrossRef]
  13. R. Bonduriansky, R. J. Brooks, Why do male antler flies (Protopiophila litigata) fight? The role of male combat in the structure of mating aggregations on moose antlers. Ethol. Ecol. Evol. 11, 287-301 (1999).
Citation: C. C. Spencer, D. E. L. Promislow, Biologists Finally Horn In on Senescence in the Wild. Science's SAGE KE (27 November 2002), http://sageke.sciencemag.org/cgi/content/full/sageke;2002/47/pe19








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