Is oxidative stress a physiological cost of reproduction? An experimental test in house mice

Abstract

Investment in reproduction is costly and frequently decreases survival or future reproductive success. However, the proximate underlying causes for this are largely unknown. Oxidative stress has been suggested as a cost of reproduction and several studies have demonstrated changes in antioxidants with reproductive investment. Here, we test whether oxidative stress is a consequence of reproduction in female house mice (Mus musculus domesticus), which have extremely high energetic demands during reproduction, particularly through lactation. Assessing oxidative damage after a long period of reproductive investment, there was no evidence of increased oxidative stress, even when females were required to defend their breeding territory. Instead, in the liver, markers of oxidative damage (malonaldehyde, protein thiols and the proportion of glutathione in the oxidized form) indicated lower oxidative stress in reproducing females when compared with non-reproductive controls. Even during peak lactation, none of the markers of oxidative damage indicated higher oxidative stress than among non-reproductive females, although a positive correlation between protein oxidation and litter mass suggested that oxidative stress may increase with fecundity. Our results indicate that changes in redox status occur during reproduction in house mice, but suggest that females use mechanisms to cope with the consequences of increased energetic demands and limit oxidative stress.

Figure 1.

Decreased oxidative damage in the livers of female house mice allowed to reproduce freely over a four-month period. Non-reproducing controls were housed with another female (non-R, open bars), while reproducing females were housed with a male either without contact of other animals (R, grey bars) or in contact with a neighbouring pair (R + TD, black bars). (a) Malonaldehyde; (b) protein thiols; (c) proportion of glutathione oxidized; (d) total glutathione. The p-values indicate a difference between groups (see electronic supplementary material, table S1).

Figure 2.

Markers of oxidative damage in the livers of female mice that had not reproduced (control, open bars), were in peak lactation (peak, grey bars) or had just weaned their litter (post, black bars). (a) Malonaldehyde; (b) total glutathione; (c) proportion of glutathione oxidized; (d) protein thiols. The p-values indicate differences between groups (see electronic supplementary material, table S1).

Figure 3.

When rearing a single litter, peak lactation females with the heaviest litters experienced the greatest protein oxidation. Spearman's rank correlations between female litter mass at peak lacatation and protein thiol content in (a) the liver (r_s = −0.86, p = 0.007) and (b) gastrocnemius muscle (r_s = −0.86, p = 0.014).