Maternal death and offspring fitness in multiple wild primates

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

Mammalian life history is marked by a strong dependent relationship between offspring and their mothers (1). The quantity or quality of maternal allocation to offspring, particularly during the gestation and lactation periods, is often related to maternal physical condition, and a range of offspring fitness outcomes are compromised if gestating or lactating mothers are in poor condition (2–8). In addition, infants that experience maternal loss prior to weaning face an enormous, acute risk of death in both nonhuman mammals and in humans (9–13) (Fig. 1, blue arrow).Open in a separate windowFig. 1.Four ways in which the death of a female primate mother (M) may be linked to her offspring’s fitness (F₁), if the death of M occurs while F₁ is still dependent on M. First, F₁ should display reduced survival during the immature period, following the death of M (especially before weaning but also after), because F₁ will lack the critically important social, nutritional, and/or protective resources that M provided (blue arrow). Second, F₁ should display reduced survival in the period before M actually dies, because, on average, mothers are in worse condition shortly before their death compared to mothers that survive the same period. We therefore expect M to provide lower-quality maternal care to F₁ during the weeks to years immediately preceding M’s death (purple arrow). Third, if F₁ survives these first two challenges, she is likely to be in chronically worse condition during adulthood because of reductions in maternal allocation that she received during development (red arrow). F₁ should therefore face reduced survival in adulthood, years (or even decades) after the death of M occurred. Fourth, this chronic reduction in F₁’s condition may have an intergenerational effect, such that F₂ (F₁’s offspring) also experience reduced immature survival (gold arrow). The blue and red arrows have been previously tested in several species; the analyses presented here focus on the purple and gold arrows.In some species, including primates, hyenas, whales, and some ungulates, mothers and offspring continue to associate after weaning, and mothers may provide substantial social and energetic input as well as protection during some or all of the remainder of the predispersal, immature period (hereafter the “immature period”) (12, 14–21). Thus, loss of the mother can continue to heighten the risk of death even in weaned, immature offspring (17, 19, 21) (Fig. 1, blue arrow). However, because offspring are less dependent on mothers during this phase of life, the effects of maternal loss after weaning can be sublethal (9, 16, 22). If an offspring that is weaned (but still partially dependent on its mother) survives its mother’s death, the offspring may experience long-lasting negative effects, including adverse behavioral or social outcomes in adolescence or adulthood [humans (23, 24); nonhumans (19, 20, 25–31)]. In baboons, chimpanzees, and elephants, motherless offspring may experience reduced survival during adolescence and adulthood, well after the maternal loss occurs, presumably because maternal loss results in a chronic reduction in body condition (13, 21, 26, 32) (Fig. 1, red arrow).These observations (see citations in previous paragraphs) combine to provide a strong framework that describes the dependent relationship between mammalian offspring and their mothers and allows us to make predictions about the expected effects of maternal death on offspring fitness. This framework relies on the following assumptions, which are based on the observations described above: Mammalian offspring are critically dependent on their mothers for nutrition, protection, transport, and learning. In many species, the period of dependence is not restricted to infancy and may extend well past weaning. During this dependent period, poor maternal body condition (defined here as an unmeasured physical state that predicts an animals’ ability to perform functions necessary for reproduction and survival) can lead to reduced maternal allocation to offspring and hence poor offspring body condition. Poor offspring condition, in turn, may have both immediate and later-life consequences for offspring fitness outcomes, including survival. As a result, mothers in poor condition (even those that survive to wean their offspring) are likely to produce offspring in poor condition that experience compromised survival. Maternal death at any time during this dependent period can therefore result in both short-term and chronic reductions in offspring physical condition and survival.This framework yields four main predictions about how maternal death experienced in early life affects offspring fitness outcomes across the life span. First, immature offspring that lose their mother will face reduced survival throughout the remainder of their immature period (Fig. 1, blue arrow). Although the impact of maternal loss will be especially strong if the mother dies before the offspring is weaned, the immature offspring may continue to face reduced survival if its mother dies any time before the offspring matures. Second, because the loss of the mother in early life results in developmental constraints that persist throughout the offspring’s lifetime, offspring that experienced early maternal loss will continue to experience reduced survival in adulthood, leading to shortened adult life spans (Fig. 1, red arrow). These two predictions are important for offspring fitness outcomes; they have been previously tested in several species (see above summary) and are therefore not the focus of our study.We focus instead on two additional predictions, which have received little previous attention. First, we expect offspring to face reduced survival if their mothers are going to die in the near future, because, on average, a mother whose death is imminent is more likely to be in poor condition compared to those mothers that survive the same period. Thus, in this prediction, imminent maternal death serves as a proxy for poor maternal condition. We can test this prediction by measuring the association between offspring survival and impending maternal death, while the mother is still alive (Fig. 1, purple arrow). Second, we predict an intergenerational effect of early maternal loss on offspring survival (Fig. 1, gold arrow). That is, we predict that female offspring that experience maternal loss but still survive to adulthood (F₁ generation in Fig. 1) will produce offspring with compromised survival (F₂ generation). We expect the proximate mechanism leading to this intergenerational effect to be that F₁’s compromised condition causes her to be less able to allocate adequate resources to her offspring.These latter two predictions about survival patterns have been previously confirmed in wild baboons (33), but otherwise we have little knowledge of the generality of these two links between maternal survival and the survival of offspring (F₁ generation) and grand offspring (F₂ generation) in natural populations of primates or other mammals. Here, we leverage long-term longitudinal data from eight wild populations of seven primate species to assess 1) the extent to which offspring suffer reduced survival when their mothers will soon die (Fig. 1, purple arrow), and 2) the extent to which the effects of early maternal loss carry over from one generation to the next, resulting in reduced immature survival for offspring whose mothers experienced early maternal loss (Fig. 1, gold arrow).