Abstract
Maternal age has a negative effect on offspring lifespan in a range of taxa and is hypothesized to influence the evolution of aging. However, the mechanisms of maternal age effects are unknown, and it remains unclear if maternal age alters offspring response to therapeutic interventions to aging. Here, we evaluate maternal age effects on offspring lifespan, reproduction, and the response to caloric restriction, and investigate maternal investment as a source of maternal age effects using the rotifer, Brachionus manjavacas, an aquatic invertebrate. We found that offspring lifespan and fecundity decline with increasing maternal age. Caloric restriction increases lifespan in all offspring, but the magnitude of lifespan extension is greater in the offspring from older mothers. The trade-off between reproduction and lifespan extension under low food conditions expected by life history theory is observed in young-mother offspring, but not in old-mother offspring. Age-related changes in maternal resource allocation to reproduction do not drive changes in offspring fitness or plasticity under caloric restriction in B. manjavacas. Our results suggest that the declines in reproduction in old-mother offspring negate the evolutionary fitness benefits of lifespan extension under caloric restriction.
Highlights
Maternal effects occur when the environment or physiological state of a mother changes the phenotype of her offspring without a corresponding change in genotype
While there has been some investigation of how genetic background may affect the response to lifespan-extending interventions such as caloric restriction, gene knockdown, or pharmaceuticals[50,51,52,53], little is known about how maternal age may influence offspring response to these therapies, or if such interventions might rescue offspring from the negative effects of maternal age
We investigated the combined effect of maternal age and offspring diet to determine (1) whether changes in gross maternal reproductive investment with increasing maternal age are correlated with offspring survivorship; (2) the extent to which increasing maternal age changes offspring response to the well-studied anti-aging therapy of caloric restriction; and (3) how maternal age and offspring diet interact to determine offspring relative age-specific reproduction as a measure of evolutionary fitness
Summary
Maternal effects occur when the environment or physiological state of a mother changes the phenotype of her offspring without a corresponding change in genotype. Lifespan, and stress resistance with increasing maternal age have since been demonstrated across taxa, ranging from invertebrates like soil mites and Drosophila, to mammals including mice and humans[26,27,29,30,31,32,34,35,36] The mechanisms of these maternal age effects are unclear, and have variously been attributed to increases or decreases in maternal investment in reproduction with increasing maternal age, as well as to other, as yet undefined, epigenetic factors[37,38,39,40,41,42,43,44]. While there has been some investigation of how genetic background may affect the response to lifespan-extending interventions such as caloric restriction, gene knockdown, or pharmaceuticals[50,51,52,53], little is known about how maternal age may influence offspring response to these therapies, or if such interventions might rescue offspring from the negative effects of maternal age
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