Leptin increases maternal investment

Abstract

The primary goal of virtually all organisms is to produce genetic offspring, thereby passing on their genes to future generations. Offspring production, however, is limited by available resources within an environment. Moreover, distributing sufficient energy among competing physiological systems is challenging and can result in trade-offs between self-maintenance and offspring investment when resources are limited. In the current study, we tested the hypothesis that the adipose hormone leptin is involved in mediating energetic trade-offs between competing physiological systems. Specifically, we tested the effects of elevated maternal leptin on investment into offspring production versus self maintenance (immune function), in the Siberian hamster (Phodopus sungorus). The current study provides the first evidence that leptin serves as a signal to mothers of available energy resulting in epigenetic effects. Therefore, elevated leptin allows females to retain more embryos to parturition, and rear more offspring to weaning via reduced maternal infanticide. Innate immune response was suppressed seemingly as a result of these enlarged litters, suggesting that the observed fitness increase is not without costs to the mother. Collectively, these findings suggest that leptin plays a critical role in allowing mothers to determine how much energy to invest in the production and care of young versus self-maintenance.

Figure 1.

Circulating leptin concentrations. Leptin is significantly elevated in leptin-treated individuals compared with vehicle-treated individuals. Leptin is also significantly lower in pregnant individuals relative to control individuals. Different letters denote groups that differ significantly (α = 0.05 level). Error bars represent ±1 s.e.

Figure 2.

Effects of leptin treatment on reproductive output. Females treated with leptin had significantly (a) more pups, (b) maintained larger litters via suppressed maternal infanticide and (c) larger final litter size (i.e. at the termination of study) than vehicle-treated control females. Asterisks denote statistically significant differences (α = 0.05 level). Error bars represent ±1 s.e.

Figure 3.

Food intake over time. There was a significant difference in food intake among treatments for ‘post-pump’ intake and a significant time × treatment interaction for ‘pre-day 10 bleed’ and ‘post-pump’ intake periods. Food intake changed significantly over time in all the analyses. Leptin-treated animals in both groups increase their food intake to a greater degree than vehicle-treated animals after the pumps stop delivering leptin, suggesting that leptin treatment was suppressing intake. Filled circles, control vehicle; open circles, control leptin; filled triangles, pregnant vehicle; open triangles, pregnant leptin. Asterisks denote statistically significant differences (α = 0.05 level). Error bars represent ±1 s.e.

Figure 4.

Effects of leptin treatment and pregnancy on maternal antibody production. Pregnant females had significantly elevated anti-KLH IgM (a) production compared with control animals. There was no significant difference in anti-KLH IgG (b) among groups; however, IgG antibodies are delivered passively to the offspring via lactation which could explain the absence of a difference among pregnant and control females. In addition, pups from leptin-treated mothers trended towards having decreased anti-KLH IgG when compared with pups from vehicle-treated mothers (p = 0.06). Asterisks denote statistically significant differences (α = 0.05 level). Error bars represent ±1 s.e.

Figure 5.

Effects of leptin treatment on bactericidal capacity. Pregnant females treated with leptin had significantly lower bacterial killing ability than all other treatments. Differing letters denote groups that differ significantly (α = 0.05 level). Error bars represent ±1 s.e.