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

Date Published: March 22, 2017

Publisher: Public Library of Science

Author(s): Adam Dušek, Luděk Bartoš, František Sedláček, I. Anna S. Olsson.

http://doi.org/10.1371/journal.pone.0173985

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.

Partial Text

The choice of strategies made by organisms in order to increase their lifetime reproductive fitness is a central issue of life-history evolution [1,2]. Female mammals have evolved a number of state-dependent life-history tactics to increase their fitness prospects [3,4]. An optimal reproductive tactic is defined as a strategy that maximizes an individual’s reproductive value (i.e. age-specific expectation of all present and future offspring) at every age [5]. A function of an individual’s reproductive value is reproductive effort, reflecting the proportional allocation of available time and energy to reproduction [6]. In female mammals, parental effort (i.e. total parental investment) typically increases with the resources available [7]. Therefore, in polytocous (litter-bearing) species, litter size is one of the most reliable state-dependent life-history traits that indicate an individual’s parental effort.

In total, 72 of the 75 (96.00%) AL-fed and 65 of the 77 (84.42%) FR female mice littered successfully. Of these, litter reduction occurred in 19 of the 72 (26.39%) AL-fed and in 24 of the 65 (36.92%) FR families. Altogether 56 of the 275 (20.36%) offspring of the AL-fed mothers and 49 of the 351 (13.96%) offspring of the FR mothers died during the lactation period. We observed the loss of the entire litter in 2 of the 19 (10.53%) AL-fed controls.

This is the first study to focus on the role of pre-breeding resource limitations for the optimization of female parental investment during the lactation period. We observed that the exposure of female mice to pre-breeding FR improved the optimization of their litter size. The FR mothers could therefore invest more efficiently in their offspring than the AL-fed mothers. As a consequence of this, the offspring of the FR mothers were in better condition and suffered less from pre-weaning mortality than those of the AL-fed mothers. Our results thus indicate, that pre-breeding FR had wide-ranging long-term effects on parental investment and offspring developmental success (i.e. increased growth and decreased mortality). These findings correspond to previous studies [35–38] suggesting the potentially beneficial effect of FR on female reproductive fitness. The complex optimization of litter size reflects the r-selected life-history, which primarily involves the maximization of offspring numbers in an unpredictable environment. This parental investment strategy may therefore explain why we observed no effects of offspring sex and litter sex ratio during the course of lactation.

Our study shows that pre-breeding FR stimulated lactating mice towards effective parental investment. This resulted in a dichotomy of reproductive optima (see Fig 9 – summarizing diagram). Exposing female mice to unpredictable food availability induced highly selective litter reduction that improved their fitness prospects. In contrast, the control females fed ad libitum produced litters of super-optimal size and thus incurred higher reproductive costs, including a greater reduction of their litters. We believe that our findings may have important implications for the understanding of the mechanisms of life-history evolution, as well as potentially for animal breeding and for research into the negative effects of obesity on reproduction. To fully evaluate the significance of these findings, future research should: (1) examine the influence of environmental uncertainty on parental fitness in natural populations of mammals; (2) determine whether pre-breeding resource limitations can benefit caring parents and their dependent offspring in a changeable environment; and (3) identify the genes and pathways involved in the optimization of parental investment.

 

Source:

http://doi.org/10.1371/journal.pone.0173985

 

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