Most evolutionary theories of aging attempt to explain the general rule, namely, most organisms become less fit as they age. The dominant theories, distinct but not entirely in competition with one another, invoke either antagonistic pleiotropy (genes that cause deleterious consequences in late life can be positively selected so long as they provide benefits early in life) or the disposable soma (in a dangerous world that poses a constant risk of exogenous mortality, it’s better to devote resources to reproduction than repair). Both theories rely on the idea that early reproduction increases fitness more than late reproduction, and that the strength of selection diminishes with age. Both theories make compelling population-genetic predictions, and the data — though scarce — generally fall in line with one or the other if not both.

What, then, do we make of organisms like redwood trees and hydras (and possibly whales), which live fantastically long lives and possibly avoid aging altogether? A valid evolutionary theory must explain these exceptions, as well as the more general case.

In a fairly densely written mathematical paper, Seymour and Doncaster attempt to answer this question. Their model accepts the basic foundations of population genetics (costly reproduction, a constant risk of mortality from endogenous and exogenous causes) and refrains from invoking any peculiar gimmicks (like ever-increasing fecundity, which can change the math regarding how the strength of selection changes with age). They find that in situations where the rate of maturation depends inversely on the population density — i.e., where more nearby adults means slower maturation for young organisms — natural selection can lead to negligible senescence. (In reading the abstract, it is useful to know that “recruitment” refers to the transition from non-reproducing juvenile to reproduction-competent adult):

Density Dependence Triggers Runaway Selection of Reduced Senescence

In the presence of exogenous mortality risks, future reproduction by an individual is worth less than present reproduction to its fitness. Senescent aging thus results inevitably from transferring net fertility into younger ages. Some long-lived organisms appear to defy theory, however, presenting negligible senescence (e.g., hydra) and extended lifespans (e.g., Bristlecone Pine). Here, we investigate the possibility that the onset of vitality loss can be delayed indefinitely, even accepting the abundant evidence that reproduction is intrinsically costly to survival. For an environment with constant hazard, we establish that natural selection itself contributes to increasing density-dependent recruitment losses. We then develop a generalized model of accelerating vitality loss for analyzing fitness optima as a tradeoff between compression and spread in the age profile of net fertility. Across a realistic spectrum of senescent age profiles, density regulation of recruitment can trigger runaway selection for ever-reducing senescence. This novel prediction applies without requirement for special life-history characteristics such as indeterminate somatic growth or increasing fecundity with age. The evolution of nonsenescence from senescence is robust to the presence of exogenous adult mortality, which tends instead to increase the age-independent component of vitality loss. We simulate examples of runaway selection leading to negligible senescence and even intrinsic immortality.

The Results section describes the authors’ assumptions and insights and sets up a mathematically rigorous model. It would be slow going for a non-quantitative reader, but not hard to follow with a bit of patience — and perhaps a willingness to dust off the old calculus and diff-eq texts in that box we all have in a closet somewhere.

For those with dust allergies or more pressing business, however, the Discussion is well-written and accessible to a more general audience. The authors describe in detail two organisms — the Bristlecone pine and Arctic quahog — that exhibit density-dependent recruitment. In both species, sessile adults live in crowded but stable conditions in which new opportunities for maturation arise rarely. In such situations, it behooves an individual organism to outlive its neighbors, so that when they die its seedlings or larvae have a place to dig in and grow up. In such contexts, the authors argue, natural selection can trigger an anti-aging arms race that results in negligible senescence as a consequence of runaway selection.

The article also contains also some interesting thoughts about the ramifications of such evolutionary forces for non-sessile organisms with unusual life histories, but I’m going to save that for next week. Watch this space for developments.

(UPDATE 2008.01.29: For more about the evolution of negligible senescence in insects and mammals, see part II).