The Challenges of Senescence for Adult Male Chimpanzees

Abstract

All animals eventually die. For many, death comes early from external sources of mortality, such as predation, whereas for others, there is a chance to grow old. These aging organisms experience senescence, the declines in vitality and function with age. While senescence reduces survival and reproduction, many individuals persist and even successfully reproduce in their advanced age. How have evolutionary forces shaped senescence, and what does growing old look like in natural settings? How do animals compensate for senescence and continue to reproduce? Addressing these questions is key to understanding how natural selection shapes variation in longevity and other life history traits across species. Such forces may have been particularly important in the evolution of primates as especially long-lived mammals, and humans even more so. One of our closest living relatives, chimpanzees (Pan troglodytes), are especially long-lived and exhibit senescence across multiple dimensions. Aging male chimpanzees decline in rank, lose weight, reproduce less, and show shifts in social behavior. Yet in other ways, these males appear to “age gracefully” as they maintain certain measures of body condition, activity, and continue to sire offspring. What are the signs of growing old for male chimpanzees from a behavioral, ecological, and energetic perspective? What tradeoffs shape the continued reproductive effort of old males? To address these questions and contribute to our understanding of the evolution of longevity, I studied a particularly long-lived cohort of 20 adult male chimpanzees (21-53 years old) over one year at Ngogo in Kibale National Park, Uganda. I found that old chimpanzees ate more slowly and processed less of their ingested food, which indicates that foraging senescence may shape the energetic profiles of old chimpanzees as a functional decline. To understand life history tradeoffs with age, I examined a suite of physiological and behavioral measures. During a food abundant period, old male chimpanzees showed no declines in energetic status or testosterone, and they climbed trees just as often as did younger adult males. But old males spent less time moving and more time resting than did younger individuals. When controlling for important factors such as rank, the social displays of old males were less frequent and covered shorter distances. And in times of food abundance, old males copulated less often than their younger counterparts. These results suggest that old male chimpanzees may strategically restrict activity to maintain reproductive condition, while engaging less in reproductive behaviors overall. Such findings provide a proximate explanation for why despite seemingly maintaining body condition, old male chimpanzees reproduce less. I also investigated social aging and found that various affiliative behaviors increased with age. Proximity to other adult males and grooming time increased with age, but only during high-quality diet periods, which could suggest that resource constraints shape the sociality of old chimpanzees. I also discuss preliminary evidence that old male chimpanzees adopt alternative reproductive tactics in the face of changing payoffs. As male chimpanzees age, foraging senescence and other deteriorations may generate new tradeoffs, yet males appear able to compensate by shifting their behaviors. These results help us understand the evolution of aging and longevity in humans and other long-lived primates.