Maternal senescence is the detrimental effect of increased maternal age on offspring performance. Despite much recent interest given to describing this phenomenon, its distribution across animal species is poorly understood. A review of the published literature finds that maternal age affects pre-adult survival in 252 of 272 populations (93%) representing 97 animal species. Age effects tended to be deleterious in invertebrates and mammals, including humans, confirming the presence of senescence. However, bird species were a conspicuous exception, as pre-adult survival tended to increase with maternal age in surveyed populations. In all groups, maternal-age effects became more negative in older mothers. Invertebrates senesced faster than vertebrates, and humans aged faster than non-human mammals. Within invertebrates, lepidopterans demonstrated the most extreme rates of maternal-effect senescence. Among the surveyed studies, phylogeny, life history and environment (e.g. laboratory versus wild populations) were tightly associated; this made it difficult to make confident inferences regarding the causes of diversity for the phenomenon. However, we provide some testable suggestions, and we observe that some differences appear to be consistent with predictions from evolutionary theory. We discuss how future work may help clarify ultimate and proximate causes for this diversity.
Maternal effect senescence has attracted much recent scientific interest. However, the age-related effects of pre-and postnatal maternal age are often conflated, as these naturally originate from the same individual. Additionally, many maternal effect senescence studies fail to account for potential biases associated with selective disappearance. Here we use a cross-fostered laboratory population of a burying beetle, Nicrophorus vespilloides, to examine both the effects of female pre-and postnatal maternal age on offspring life-history traits and the postcare outcomes of mothers while accounting for selective disappearance of postnatal caregivers. Neither pre-nor postnatal maternal age affected offspring longevity or larval weight at hatching, and postnatal age had no effect on postcare maternal outcomes except to confirm the presence of actuarial senescence. There was weak evidence for concave relationships between two larval traits (dispersal weight and survival) and the age of egg producers. Selective disappearance of caregivers had no clear effect on any of the measured offspring traits. Contrary to predictions from evolutionary theory, maternal effect senescence and reproductive effort increases do not always manifest, and current theory may be insufficient to account for the true diversity of aging patterns relating to maternal care.
The theory that ageing evolves because of competitive resource allocation between the soma and the germline has been challenged by studies showing that somatic maintenance can be improved without impairing reproduction. However, it has been suggested that cost‐free improvement in somatic maintenance is possible only under a narrow range of benign conditions. Here, we show that experimental downregulation of insulin/IGF‐1 signaling (IIS) in C. elegans nematodes, a robustly reproducible life span‐ and health span‐extending treatment, reduces fitness in a complex variable environment when initiated during development but does not reduce fitness when initiated in adulthood. Thus, our results show that the costs and benefits of reduced IIS can be uncoupled when organisms inhabit variable environments, and, therefore, do not provide support for the resource allocation theory. Our findings support the theory that the force of natural selection on gene expression in evolutionarily conserved signaling pathways that shape life‐history traits declines after the onset of reproduction resulting in organismal senescence.
Dietary restriction (DR) improves survival across a wide range of taxa yet remains poorly understood. The key unresolved question is whether this evolutionarily conserved response to temporary lack of food is adaptive. Recent work suggests that early-life DR reduces survival and reproduction when nutrients subsequently become plentiful, thereby challenging adaptive explanations. A new hypothesis maintains that increased survival under DR results from reduced costs of overfeeding. We tested the adaptive value of DR response in an outbred population of Drosophila melanogaster fruit flies. We found that DR females did not suffer from reduced survival upon subsequent re-feeding and had increased reproduction and mating success compared to their continuously fully fed (FF) counterparts. The increase in post-DR reproductive performance was of sufficient magnitude that females experiencing early-life DR had the same total fecundity as continuously FF individuals. Our results suggest that the DR response is adaptive and increases fitness when temporary food shortages cease.
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