Untangling the oxidative cost of reproduction: An analysis in wild banded mongooses

Abstract

The cost of reproduction plays a central role in evolutionary theory, but the identity of the underlying mechanisms remains a puzzle. Oxidative stress has been hypothesized to be a proximate mechanism that may explain the cost of reproduction. We examine three pathways by which oxidative stress could shape reproduction. The “oxidative cost” hypothesis proposes that reproductive effort generates oxidative stress, while the “oxidative constraint” and “oxidative shielding” hypotheses suggest that mothers mitigate such costs through reducing reproductive effort or by pre‐emptively decreasing damage levels, respectively. We tested these three mechanisms using data from a long‐term food provisioning experiment on wild female banded mongooses (Mungos mungo). Our results show that maternal supplementation did not influence oxidative stress levels, or the production and survival of offspring. However, we found that two of the oxidative mechanisms co‐occur during reproduction. There was evidence of an oxidative challenge associated with reproduction that mothers attempted to mitigate by reducing damage levels during breeding. This mitigation is likely to be of crucial importance, as long‐term offspring survival was negatively impacted by maternal oxidative stress. This study demonstrates the value of longitudinal studies of wild animals in order to highlight the interconnected oxidative mechanisms that shape the cost of reproduction.

Defence against the intergenerational cost of reproduction in males: oxidative shielding of the germline

“…1). Indeed, single‐time‐point measurements of oxidative stress markers during a reproductive event can give a misleading picture of the oxidative costs associated with reproduction (Meniri et al ., 2022). Comparison between breeders and non‐breeders can validate the expectation that transition to reproduction incurs a decrease in oxidative damage levels; damage levels are expected to remain relatively consistent over time in non‐breeders.…”

“…Previous work has linked maternal oxidative damage to impacts on offspring survival. Higher maternal oxidative resistance in alpine swifts (Apus melba) (Bize et al, 2008) and lower maternal oxidative damage in banded mongooses (Mungos mungo) (Vitikainen et al, 2016) and common lizards (Zootoca vivipara) (Dupoué et al, 2020) were associated with increased offspring survival, although a follow-up study on banded mongooses (Meniri et al, 2022) showed this result was dependent on the type of maternal damage measured. Lipid oxidative damage was negatively correlated with offspring survival while protein oxidative damage showed the opposite pattern (Meniri et al, 2022).…”

“…Higher maternal oxidative resistance in alpine swifts (Apus melba) (Bize et al, 2008) and lower maternal oxidative damage in banded mongooses (Mungos mungo) (Vitikainen et al, 2016) and common lizards (Zootoca vivipara) (Dupoué et al, 2020) were associated with increased offspring survival, although a follow-up study on banded mongooses (Meniri et al, 2022) showed this result was dependent on the type of maternal damage measured. Lipid oxidative damage was negatively correlated with offspring survival while protein oxidative damage showed the opposite pattern (Meniri et al, 2022). Maternal oxidative damage has also been connected to offspring reproductive fitness: greater oxidative damage was associated with reduced breeding success of daughters in Japanese quail (Coturnix japonica) (Romero-Haro, Pérez-Rodríguez & Tschirren, 2022).…”

“…Incorporating this intergenerational perspective may be key to understanding why levels of oxidative damage have been found to become either diminished or remain stable during reproduction (Blount et al, 2016). For example, reductions in oxidative damage in breeding female banded mongooses are associated with enhanced offspring survival (Vitikainen et al, 2016;Meniri et al, 2022), although the same pattern was not found in Columbian ground squirrels (Urocitellus columbianus) (Viblanc et al, 2018).…”

Corrigendum

“…In the recent article by Meniri et al ( 2022 ), the survival effect was interpreted the wrong way around, with a positive effect on survival interpreted as a negative one in Figure 6. The author would like to amend the result section and the associated paragraph in the discussion where they interpret this result.…”