Pre-breeding food restriction promotes the optimization of parental investment in house mice, Mus musculus

Abstract

Litter size is one of the most reliable state-dependent life-history traits that indicate parental investment in polytocous (litter-bearing) mammals. The tendency to optimize litter size typically increases with decreasing availability of resources during the period of parental investment. To determine whether this tactic is also influenced by resource limitations prior to reproduction, we examined the effect of experimental, pre-breeding food restriction on the optimization of parental investment in lactating mice. First, we investigated the optimization of litter size in 65 experimental and 72 control families (mothers and their dependent offspring). Further, we evaluated pre-weaning offspring mortality, and the relationships between maternal and offspring condition (body weight), as well as offspring mortality, in 24 experimental and 19 control families with litter reduction (the death of one or more offspring). Assuming that pre-breeding food restriction would signal unpredictable food availability, we hypothesized that the optimization of parental investment would be more effective in the experimental rather than in the control mice. In comparison to the controls, the experimental mice produced larger litters and had a more selective (size-dependent) offspring mortality and thus lower litter reduction (the proportion of offspring deaths). Selective litter reduction helped the experimental mothers to maintain their own optimum condition, thereby improving the condition and, indirectly, the survival of their remaining offspring. Hence, pre-breeding resource limitations may have facilitated the mice to optimize their inclusive fitness. On the other hand, in the control females, the absence of environmental cues indicating a risky environment led to "maternal optimism" (overemphasizing good conditions at the time of breeding), which resulted in the production of litters of super-optimal size and consequently higher reproductive costs during lactation, including higher offspring mortality. Our study therefore provides the first evidence that pre-breeding food restriction promotes the optimization of parental investment, including offspring number and developmental success.

Fig 1. Schematic diagram of the experimental setup.

The hypothesized effect of the pre-breeding feeding treatment of the female (ad libitum–AL, food restriction–FR) on the optimization of her parental investment during lactation. Considering the changes that may occur with time, we investigated this effect over the course of five equal lactation periods.

Fig 2. Litter size at birth and at weaning.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on litter size (a) at birth and (b) at weaning in the families with and without litter reduction. Bars indicate LS-means ± S.E.; numbers above the bars indicate the sample size (*P < 0.05, **P < 0.01).

Fig 3. Total litter reduction.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on total litter reduction (proportion of all offspring deaths from day 1 to 21); numbers above the bars indicate the sample size (*P < 0.05).

Fig 4. Dynamics of offspring mortality.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on the proportions of offspring deaths in particular lactation periods; numbers above the bars indicate the sample size (*P < 0.05).

Fig 5. Maternal weight change.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on the relationships between maternal weight change and (a) prior litter size, (b) offspring weight change, and (c) litter biomass change. Only the regression lines of the significant relationships are shown.

Fig 6. Offspring weight change.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on the relationships between offspring weight change and (a) prior litter size, (b) maternal weight change, and (c) litter biomass change. Only the regression lines of the significant relationships are shown.

Fig 7. Probability of offspring death.

The effect of pre-breeding maternal feeding treatment (ad libitum–AL; food restriction–FR) on the relationships between the probability of offspring death and (a) prior litter size, (b) mother’s prior weight, (c) maternal weight change, and (d) offspring prior weight. Only the regression lines of the significant relationships are shown.

Fig 8. Interaction of maternal weight change with offspring weight.

The probability of offspring death depending on the interaction between the maternal weight change and offspring prior weight (a) in the ad libitum (AL)-fed mothers, and (b) in the food-restricted (FR) mothers.

Fig 9. Mechanisms of fitness optimization.

The impact of pre-breeding maternal feeding treatment (a: ad libitum–AL; b: food restriction–FR) on the relationships between maternal condition (mother’s prior weight, maternal weight change), offspring condition (offspring prior weight, offspring weight change), and offspring mortality (probability of offspring death, litter biomass change). The arrows indicate the directions of the significant effects of particular relationships. Positive and negative relationships are respectively denoted with + and–. The scheme demonstrates that: (1) offspring condition was only positively associated with maternal condition in the AL-fed mice; (2) maternal condition was only positively associated with offspring condition in the FR mice; and (3) offspring mortality decreased with increasing maternal and offspring condition in both groups, but only in the AL-fed mice did their condition decline with increasing offspring mortality.