The distribution of the Lansing Effect across animal species

Abstract

Maternal senescence is a reduction in individual performance associated with an increase in its mother’s age at conception. When manifested on adult lifespan, this is known as the ‘Lansing Effect’. Single-species studies report both maternal age-related increases and decreases in adult lifespan, but no comprehensive review of the literature has yet determined if the Lansing Effect is a widespread phenomenon. To address this knowledge gap, we performed a meta-analysis of maternal aging rates taken from all available published studies. We recovered 74 estimates from 20 studies representing 14 species. All studies taken together suggest a propensity for a Lansing Effect with an estimated average effect of maternal age on adult lifespan of between -22% to -17% (the lifespan response to an increase in maternal age expressed in the same time units), depending upon our specific choice of model. We failed to find a significant effect of animal class or insect order, but given the oversampling of insect species in the published literature and the paucity of vertebrate studies, we infer that only rotifers and insects demonstrate a tendency for expressing the phenomenon.

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

“…The fly experiments indicate that in a highly inbred genetic line, stochastic effects inherent to the ageing process can explain several findings that currently lack a mechanistic explanation. Offspring from older mothers show truncated lifespans, also termed the Lansing effect 17,36 . Similarly, parental and offspring lifespan correlations are often interpreted in a genetic context only 37 .…”

“…Stochasticity thus leads to an apparent trade-off between reproductive output and lifespan across individuals that are intrinsically physiologically identical (Figure 1E, F). We can further apply this model to understand the effects of parental age on offspring fitness 35 and lifespan 17 , also termed the Lansing effect. We can hypothesise either part of physiology, the reproduction or lifespan sustaining component is passed down through nongenetic inheritance.…”

“…How reproduction changes with age, often termed reproductive senescence, has also been shown to vary amongst individuals in human and other animal populations 15,16 . In addition to this there are mechanistically unexplained effects of parental age on offspring lifespan and reproduction 17,18 . Non-genetic inheritance of how organisms age is thus documented but not understood.…”

“…Note that any of these effects are unlikely due to population size differences in the growing vials, as total pupal case numbers per vial did not correlate to the resulting lifespan of offspring from those vials (rs = 0.048, P = 0.74).The fly experiments indicate that in a highly inbred genetic line, stochastic effects inherent to the ageing process can explain several findings that currently lack a mechanistic explanation. Offspring from older mothers show truncated lifespans, also termed the Lansing effect17,36 . Similarly, parental and offspring lifespan correlations are often interpreted in a genetic context only37 .…”

No time to die: Evolution of a post‐reproductive life stage

“…In considering the fitness costs of cessation of reproduction in later life, no account is generally taken of the fact that offspring produced by older parents can be of poorer quality and have reduced lifespan (termed the Lansing effect) and reproductive value (Comfort, 1953; Ivimey‐Cook et al., 2023; Lansing, 1947; Monaghan et al., 2020; Monaghan & Metcalfe, 2019). A recent meta‐analysis by Ivimey‐Cook et al.…”