Inverse Lansing effect: maternal age and provisioning affecting daughters’ longevity and male offspring production

Abstract

Maternal age effects on life history of offspring has been demonstrated in a variety of organisms, more often than not offspring of older mothers having lower life expectancy (Lansing effect). However, there is no consensus on how general this phenomenon is and what are the genetic and epigenetic mechanisms behind it. We tested the predictions of Lansing effect in several Daphnia magna clones in and observed a significant genotype-by-maternal age interaction, indicating clone-specific magnitude and direction of the effect of maternal age on daughters' longevity. We then repeated this experiment with more detailed life-history and offspring provisioning data focusing on 2 clones with contrasting life-histories. One of these clones demonstrating the inverse Lansing effect, with daughters of older mothers living longer than those of young mothers. Individuals from a single-generation maternal age reversal treatment showed intermediate lifespan. We also report genotype-specific, ambidirectional, and largely fecundity-independent effects of maternal age on daughters' propensity to produce male offspring, with daughters of older mothers showing higher male production than daughters of younger mothers in the least male-producing clone and vise versa. We tested whether both effects can be explained by either lipid provisioning of embryos by mothers of different age, or by properties of mitochondria transmitted by mothers of different age to their offspring, using rhodamine-123 assay of mitochondrial membrane potential as a measure of mitochondria quality. We show that once lipid provisioning is accounted for, the effects of maternal age on lifespan and male production disappear and that the effect of lipid provisioning itself is clone-dependent, confirming that maternal provisioning sets daughters life history parameters. In the clone showing the inverse Lansing effect we demonstrated that, contrary to the predictions, neonates produced by older mothers were characterized by higher mitochondrial membrane potential in neural tissues than their counterparts born to younger mothers. We conclude that, in at least some genotypes, a reverse Lansing effect is possible, and hypothesize that it may be a result of lower lipid provisioning creating calorically restricted environment during embryonic development.