Stochasticity Explains Nongenetic Inheritance of Lifespan and Apparent Trade-Offs between Reproduction and Aging

Stochastic effects are central to the biology and demography of aging. 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 the stochastic effects of aging 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 aging by dichotomizing aging physiology in reproduction and lifespan-supporting units. These simple models reproduce the nongenetic inheritance of lifespan, the Lansing effect, and trade-offs between reproduction and lifespan. Our work implies that if nongenetic inheritance of lifespan is widespread, it explains the generally low heritability of this trait. Furthermore, trade-offs between performance, for example, reproduction, and lifespan may be less widespread than predicted by the evolutionary biology of aging, stemming from stochasticity rather than differential investment. Antiaging treatments could therefore come without any unintended costs to other physiology, a perceived risk that limits the translation of these treatments to humans.