Senescence: Still an Unsolved Problem of Biology

Abstract

Peter Medawars An Unsolved Problem of Biology1 was one of several formal attempts to provide an explanation for the evolution of senescence, the increasing risk of mortality and decline in reproduction with age after achieving maturity. Despite ca. seven decades of theoretical elaboration aiming to explain the problem since Medawar first outlined it, we argue that this fundamental problem of biology remains unsolved. Here, we utilise demographic information2, 3 for 308 multicellular species to derive age-based trajectories of mortality and reproduction that provide evidence against the predictions of the classical, still prevailing, theories of ageing1, 4, 5, 6. These theories predict the inescapability of senescence1, 4, or its universality at least among species with a clear germ-soma barrier5, 6. The patterns of senescence in animals and plants that we report contradict both of these predictions. With the largest ageing comparative dataset of these characteristics to date, we build on recent evidence7, 8 to show that senescence is not the rule, and highlight the discrepancy between existing evidence and theory7, 8, 9. We also show that species age patterns of mortality and reproduction often follow divergent patterns, suggesting that organisms may display senescence for one component but not the other. We propose that ageing research will benefit from widening its classical theories beyond merely individual chronological age; key life history traits such as size, the ecology of the organism, and kin selection, may together play a hidden, yet integral role in shaping senescence outcomes.