Abstract
Oxidative damage has been proposed as a potential mechanism underlying a life history tradeoff between survival and reproduction. However, evidence that reproduction is associated with increased oxidative damage is equivocal, and some studies have found that breeding females exhibit reduced, rather than elevated, levels of oxidative damage compared to equivalent non-breeders. Recently it was hypothesised that oxidative damage could have negative impacts on developing offspring, and that mothers might down-regulate oxidative damage during reproduction to shield their offspring from such damage. We tested this hypothesis through a longitudinal study of adult survival, reproduction, and oxidative damage in wild banded mongooses (Mungos mungo) in Uganda. High levels of oxidative damage as measured by malondialdehyde (MDA) were associated with reduced survival in both sexes. Levels of protein carbonyls were not linked to survival. Mothers showed reduced levels of MDA during pregnancy, and individuals with higher MDA levels gestated fewer offspring and had lower pup survival. These results suggest that maternal oxidative damage has transgenerational costs, and are consistent with the idea that mothers may attempt to shield their offspring from particularly harmful types of oxidative damage during pregnancy. Further advance in understanding of life history variation would benefit from theory and tests of the potential transgenerational impacts of the mechanisms underlying life history trade-offs.
Highlights
A tenet of life history theory is the idea that investment in reproduction is costly to survival (Kirkwood and Rose, 1991; Hammers et al, 2013; Moore et al, 2013)
Opposite to the pattern expected under the OSTA, plasma levels of MDA declined with age [linear mixed model (LMM), individual and group as random effects: χ(21) = 8.03, p = 0.0046; N = 331; Figure 2A, Supplementary Table S3A]
Models of oxidative stress and damage accumulation have focused on individual schedules of mortality and fecundity, and have largely ignored its potential transgenerational impacts (Munch and Mangel, 2006; McNamara et al, 2009)
Summary
A tenet of life history theory is the idea that investment in reproduction is costly to survival (Kirkwood and Rose, 1991; Hammers et al, 2013; Moore et al, 2013). A recent meta-analysis of studies of female birds and mammals showed that there is a positive association between reproductive effort (i.e., offspring number) and oxidative damage, while paradoxically, levels of oxidative damage in certain tissues are lower in breeders compared to non-breeders of similar age and condition—the opposite pattern to that expected under OSTA (Blount et al, 2015). The predicted relationship between reproductive effort and oxidative damage will depend on the balance between maternal and transgenerational impacts of oxidative damage, and the degree to which mothers are selected to shield their offspring from harm. The model shows that mothers may be selected to reduce oxidative damage during pregnancy at the cost of damage levels during non-breeding periods; and that mothers with higher levels of damage during reproductive periods should produce smaller litters and fewer surviving young (Supplementary Figure S1)
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