Aging in Wild Female Lemurs: Sustained Fertility with Increased Infant Mortality

Abstract

Understanding the way prosimian primates age can be helpful in inferring what the 'basal primate mode' of senescence may have been. Even though prosimians are known to be long-lived in captivity, relatively little is known about their reproductive senescence, and even less is known about how prosimians age in their natural habitats. Twenty years of observational data in Madagascar for four Propithecus edwardsi sifaka groups were used to analyze reproductive and behavioral trends of aging in the wild. Techniques using tooth wear were developed to establish ages of wild sifakas and to estimate the onset of their 'dental senescence', a proxy for the onset of decline in the ability to obtain nutrition. Estimated maximum longevity was 32 years for female sifakas. Based on the loss of dental functional morphology, and changes in tooth wear patterns and in chewing efficiency, dental senescence was estimated to set in at approximately 18 years of age. Of the adult females in the study groups, the yearly average of the number of dentally senescent females was 24%. There was no indication of a decline in fertility in the dentally senescent females (aged >18 years) compared to younger adult females (aged 4-18 years). The field data showed, however, that in years when rain was decreased during months of prime lactation, infants of dentally senescent mothers died before weaning. This may be because the nursing mother's worn teeth could not shear leaves and extract moisture, nor nutrition, both essential for successful lactation. Old females showed no clear signs of social disengagement, further suggesting that drought-induced stress plays a direct role in increased infant mortality. These data support earlier findings that prosimian females continue to cycle and give birth until death. The effect of environmental variation on infant survival, however, indicates an incipient age-linked decline in reproductive fitness. Therefore, whereas lemurs represent the condition of no menopause, changes in infant survival may uncover selective factors that have in part led to the evolution of menopause in other primates.