Stochasticity explains non-genetic inheritance of lifespan and apparent trade-offs between reproduction and ageing

Stochastic effects are central to the biology and demography of ageing. Genetically identical individuals do not all die at the exact same time but show a distribution of lifespan. Although such effects are appreciated, any cascading effects from stochastic effects of ageing are underappreciated. We show here that genetically identical female flies (Drosophila melanogaster) that live long, produce longer lived daughters. In line with previous work, we also find that daughters born to older mothers are shorter lived, also termed the Lansing effect. We further show that longer-lived flies produce less offspring, suggesting an apparent trade-off due to stochastic effects alone. We explain these effects using an extension of the reliability theory of ageing by dichotomising ageing physiology in reproduction and lifespan supporting units. These simple models reproduce non-genetic inheritance of lifespan, the Lansing effect and trade-offs between reproduction and lifespan. Our work implies that if non-genetic inheritance of lifespan is widespread it explains the generally low heritability of this trait. Furthermore, trade-offs between performance, e.g. reproduction, and lifespan may be less widespread than predicted by evolutionary biology of ageing, stemming from stochasticity rather than differential investment. Anti-ageing treatments therefore come without any unintended costs to other physiology, a perceived risk that limits translation of these treatments to humans.