Standard evolutionary theories of aging and mortality, implicitly based on assumptions of spatial averaging, hold that natural selection cannot favor shorter lifespan without direct compensating benefit to individual reproductive success. Here we show that both theory and phenomenology are consistent with programmed death. Spatial evolutionary models show that self-limited lifespan robustly results in long-term benefit to a lineage; longer-lived variants may have a reproductive advantage for many generations, but shorter lifespan ultimately confers long-term reproductive advantage through environmental feedback acting on much longer time scales. Numerous model variations produce the same qualitative result, demonstrating insensitivity to detailed assumptions; the key conditions under which self-limited lifespan is favored are spatial extent and locally exhaustible resources. Numerous empirical observations can parsimoniously be explained in terms of long-term selective advantage for intrinsic mortality. Classically anomalous empirical data on natural lifespans and intrinsic mortality, including observations of longer lifespan associated with increased predation, and evidence of programmed death in both unicellular and multicellular organisms, are consistent with specific model predictions. The generic nature of the spatial model conditions under which intrinsic mortality is favored suggests a firm theoretical basis for the idea that evolution can quite generally select for shorter lifespan directly.
Model snapshots showing different spatial distributions of consumers and resources. Resources are shown in yellow; consumers with intrinsic mortality are shown in blue, those without it in red; empty spaces are shown in black. The values of p and q for each panel are those which evolve in ascendance studies. Each panel shows 250 × 250 sites; parameter values for which populations without intrinsic mortality were not found to be stable are shown as empty lattices (details and full lattice sizes in the Models section).
Ascendance studies favor self-limited lifespan. History of evolving consumer lifespan in one example simulation, showing population mean/maximum/minimum.
A successful invasion of consumers without intrinsic mortality by those with the capacity for programmed death. Snapshots at 150, 1250, and 2350 time steps. Resources are shown in yellow; consumers with intrinsic mortality are shown in blue, those without it in red; empty spaces are shown in black.
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