Abstract

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.

Highlights

  • Senescence, usually treated as synonymous with ‘‘aging,’’ refers to a deterioration in physiological condition with age, manifest as an increase in mortality and a decline in fertility. Since this phenomenon is detrimental to reproductive success, natural selection might be expected to cause its postponement or elimination from the life history of organisms

  • Senescent aging is an irreversible deterioration in physiological condition with age, which many organisms express even when removed from harmful environmental influences

  • Since reproduction carries physiological costs, natural selection in a hazardous environment favors reaping early benefits, and delaying the cost in physiological decline until later in life when there is a greater chance of being dead from exogenous factors

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Summary

Introduction

Senescence, usually treated as synonymous with ‘‘aging,’’ refers to a deterioration in physiological condition with age, manifest as an increase in mortality and a decline in fertility. Since this phenomenon is detrimental to reproductive success, natural selection might be expected to cause its postponement or elimination from the life history of organisms. The first emphasizes the accumulation of late-acting deleterious mutations on hypothesized genes with age-specific expression [1,4] This paradigm hypothesizes an antagonistic pleiotropy of age-specific genes in which mutations confer a fitness benefit early in life at the cost of some deleterious effect later [4,5,6]. Hamilton concludes: ‘‘...for organisms that reproduce repeatedly, senescence is to be expected as an inevitable consequence of the working of natural selection’’ [4]

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