Offspring number, size, and survival: State-dependent optimization of litter size in a long-lived capital breeder

Seventy-five years ago, Lack proposed that there should be an optimal clutch size shared by all individuals in a population and favored by natural selection, which maximizes the number of recruited offspring. While some studies support this “common optimum” hypothesis, others have shown that the optimal clutch size depends on maternal state (e.g., age and body condition, “state-dependent optimization”). These contrasting results suggest that the degree of state dependency might itself depend on the ecological context (e.g., capital vs. income breeding). Furthermore, almost all these studies were conducted on fast-living species and have ignored interdependencies among variables such as maternal age and condition. Here, we test whether females share a common optimal litter size or have a state-dependent optimal litter size in a slow-paced capital breeder, the polar bear (Ursus maritimus). To do so, we assess the influences of (1) maternal state on litter size, (2) maternal state and litter size on cub mass, and (3) maternal state, litter size, and cub mass on cub survival, using path analysis to account for interdependencies among variables and capture–recapture modeling to estimate cub survival. We use 34 years (1992–2025) of individual-based data from a polar bear subpopulation in the Svalbard region of Norway. In accordance with the state-dependent optimization hypothesis, litter size varied with maternal age and size. Middle-aged and sized females had the highest probability of having twins. Old and large females more often had triplet litters. Cub mass decreased with increasing litter size, whereas litter mass increased, meaning females with a large litter allocated more resources to reproduction. Cub mass in turn strongly predicted cub survival, indicating that offspring survival was traded against offspring number. In middle-aged and old females, productivity—the number of cubs surviving their first year—increased with litter size, in accordance with the state-dependent optimization hypothesis. Overall, our results are consistent with a state-dependent optimization of litter size in this large, slow-paced mammal producing small litters. State dependence of litter size may be more likely in capital breeders as the amount of energy available for reproduction is known in advance.