Oxidative costs of reproduction in mouse strains selected for different levels of food intake and which differ in reproductive performance

Abstract

Oxidative damage caused by reactive oxygen species has been hypothesised to underpin the trade-off between reproduction and somatic maintenance, i.e., the life-history-oxidative stress theory. Previous tests of this hypothesis have proved equivocal, and it has been suggested that the variation in responses may be related to the tissues measured. Here, we measured oxidative damage (protein carbonyls, 8-OHdG) and antioxidant protection (enzymatic antioxidant activity and serum antioxidant capacity) in multiple tissues of reproductive (R) and non-reproductive (N) mice from two mouse strains selectively bred for high (H) or low (L) food intake, which differ in their reproductive performance, i.e., H mice have increased milk energy output (MEO) and wean larger pups. Levels of oxidative damage were unchanged (liver) or reduced (brain and serum) in R versus N mice, and no differences in multiple measures of oxidative protection were found between H and L mice in liver (except for Glutathione Peroxidase), brain or mammary glands. Also, there were no associations between an individual's energetic investment (e.g., MEO) and most of the oxidative stress measures detected in various tissues. These data are inconsistent with the oxidative stress theory, but were more supportive of, but not completely consistent, with the 'oxidative shielding' hypothesis.

Figure 1

Markers of oxidative stress in the serum of non-reproducing female mice (NH, black bars, N = 10; NL, dark grey bars, N = 10) and reproducing mice at day of weaning (RH, striated bars; N = 20, RL, light grey bars, N = 14) (A) Reactive oxygen metabolites (ROMs). (B) Total non-enzymatic antioxidants capacity (OXY, untransformed data). Different letters inside the bars indicate significant differences between groups.

Figure 2. Markers of enzymatic antioxidants in the liver of non-reproducing female mice (NH, black bars; NL, dark grey bars) and reproducing mice at day of weaning (RH, striated bars; RL, light grey bars).

(A) Catalase (CAT) activity. (B) Glutathione peroxidase (GPx) activity. Different letters inside the bars indicate significant differences between groups (N = 10 per group).

Figure 3

Pearson’s correlations between (A) Food intake and DNA damage (measured by ELISA) in pooled reproducing mice (RH and RL, N = 11, filled circles) and pooled non-reproducing mice (NH and NL, N = 10, open circles). Reproducing mice, R² = 0.473, P-Value = 0.142; Non-reproducing mice, R² = −0.559, P-Value = 0.093 (B) Litter mass and liver protein damage (PC) in reproducing mice, RH mice (N = 10, filled circles) and RL mice (N = 10, open circles). Regression lines for RH mice,. R² = −0.62, P-Value = 0.05. Regression line for RL mice,. R² = −046, P-Value = 0.186., (C) Litter size and liver protein damage (PC) in reproducing mice, RH mice (N = 10, filled circles) and RL mice (N = 10, open circles). RH mice, R² = 0.148, p = −0.492, RL mice, R² = 0.246. p = − 0.404.

Figure 4. Markers of oxidative damage and enzymatic antioxidant in the brain of non-reproducing female mice (NH, black bars; NL, dark grey bars) and reproducing mice at day of weaning (RH, striated bars; RL, light grey bars, N = 10 for each group).

(A) Protein carbonyls (PC, untransformed data). (B) Catalase (CAT, untransformed data) activity. Different letters inside the bars indicate significant differences.