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.

Maternal age effects on offspring lifespan and reproduction vary within a species

“…Thus, the authors concluded that increased early life reproduction traded-off with lifespan and that maternal age effects were a result of better offspring provisioning by older mothers. Similarly, Anderson and colleagues [20] studied multiple strains of Daphnia magna and found an “inverse Lansing Effect” in some strains, in which offspring of older mothers lived longer than offspring of younger mothers. They hypothesized that this inverse effect could be a result of decreased lipid offspring provisioning by older mothers, which could result in embryonic caloric restriction.…”

“…In Daphnia pulex , advanced maternal age decreased offspring lifespan in two of three clones studied, but advanced maternal age led to higher growth rates in offspring in all three clones [19]. In Daphnia magna , five clones showed positive, negative, and neutral maternal age effects on lifespan [20]. Such high intraspecific variability in maternal age effects within these model arthropods and rotifers demonstrates the importance of including multiple strains or populations in future studies of maternal age effects in other clades.…”

“…Analyses among species are limited by multiple confounding variables, but within species we can compare populations or strains with relatively similar genetics, morphology, life history strategies, and environments, but distinct vital rates. Studies of Daphnia [19,20], Drosophila [4,11,21,22], and other insects [23] provide examples of high variability in the magnitude and direction of parental age effects on lifespan, development, fecundity, or embryonic diapause among strains and populations. To understand whether intraspecific variability in maternal age effects is typical, additional experimental studies of other clades are needed.…”

Post-senescence reproductive rebound inDaphniaassociated with reversal of age-related transcriptional changes

“…In this study we focus on the regularly occurring cases of late-life restoration of reproductive function in Daphnia - a freshwater planktonic crustacean that is a classic model organism in aging and longevity research (Ingle 1933), which is enjoying a revival due to contemporary genomic tools (Miner et al 2012), generating a significant new data on aging (Schumpert et al 2015; Constantinou et al 2019; Cai et al 2020; Hearn et a; 2021; Nguyen et al 2021; Anderson et al 2022; Cho et al 2022). Daphnia are particularly suitable for cohort longevity and reproductive senescence studies because their reproduction mode, the cyclic parthenogenesis, allows to create cohorts of genetically identical and yet fully outbred individuals, thus providing an advantage over the use of inbred lined customary in Drosophila or C. elegans longevity studies.…”

“…Our previous studies on aging hallmarks in Daphnia indicate that mitochondrial dysfunction is an unlikely cause of aging (and therefore its reversal an unlikely cause of reproductive rejuvenation), as little if any reduction of respiratory activity of mitochondrial membrane potential occurs at old age (Anderson et al 2022). On the other hand, accumulation of oxidized lipids and misfolded proteins in the forms of lipofucsins and amyloids has been shown to increase with age (Lowman & Yampolsky 2023).…”