Diane K. Brockman

Aging in the Natural World: Comparative Data Reveal Similar Mortality Patterns Across Primates

Aging patterns in humans fall within the parameters of other primates in natural populations. Human senescence patterns—late onset of mortality increase, slow mortality acceleration, and exceptional longevity—are often described as unique in the animal world. Using an individual-based data set from longitudinal studies of wild populations of seven primate species, we show that contrary to assumptions of human uniqueness, human senescence falls within the primate continuum of aging; the tendency for males to have shorter life spans and higher age-specific mortality than females throughout much of adulthood is a common feature in many, but not all, primates; and the aging profiles of primate species do not reflect phylogenetic position. These findings suggest that mortality patterns in primates are shaped by local selective forces rather than phylogenetic history.

Reproductive aging patterns in primates reveal that humans are distinct

Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.

Low Demographic Variability in Wild Primate Populations: Fitness Impacts of Variation, Covariation, and Serial Correlation in Vital Rates

In a stochastic environment, long‐term fitness can be influenced by variation, covariation, and serial correlation in vital rates (survival and fertility). Yet no study of an animal population has parsed the contributions of these three aspects of variability to long‐term fitness. We do so using a unique database that includes complete life‐history information for wild‐living individuals of seven primate species that have been the subjects of long‐term (22–45 years) behavioral studies. Overall, the estimated levels of vital rate variation had only minor effects on long‐term fitness, and the effects of vital rate covariation and serial correlation were even weaker. To explore why, we compared estimated variances of adult survival in primates with values for other vertebrates in the literature and found that adult survival is significantly less variable in primates than it is in the other vertebrates. Finally, we tested the prediction that adult survival, because it more strongly influences fitness in a constant environment, will be less variable than newborn survival, and we found only mixed support for the prediction. Our results suggest that wild primates may be buffered against detrimental fitness effects of environmental stochasticity by their highly developed cognitive abilities, social networks, and broad, flexible diets.

Evidence of Invasive Felis silvestris Predation on Propithecus verreauxi at Beza Mahafaly Special Reserve, Madagascar

Increasing evidence supports the idea that endemic avian and mammalian predators have profoundly impacted primate populations in Madagascar (Goodman, S. M. Predation on lemurs. In S. M. Goodman, & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1221–1228). Chicago: University of Chicago Press, (2003).). The role in regulating lemur populations of the 3 introduced mammalian carnivorans —small Indian civets (Viverricula indica, Desmarest 1804), domestic dogs (Canis lupus familiaris, Linnaeus 1758), and invasive wildcats (Felis silvestris, Schreber 1775)— is less clear, but recent evidence suggests that the latter 2 are becoming important predators of diurnal lemurs. We report evidence for invasive wildcat predation on sifaka (Propithecus verreauxi verreauxi) in Parcel 1 at Beza Mahafaly Special Reserve, Madagascar, including skeletal remains of apparent Propithecus sifaka victims, observations of wildcat predatory behavior, and behavioral responses of the lemurs in the presence of wildcats.

Beza Mahafaly Special Reserve: Long-Term Research on Lemurs in Southwestern Madagascar

The Beza Mahafaly Project in southwestern Madagascar was founded in 1975. It was established as a collaborative effort among the University of Madagascar (now University of Antananarivo), Washington University, Yale University, and the local communities for long-term training and research, biodiversity conservation, and socioeconomic development. Beza Mahafaly consists of two noncontiguous forest parcels separated by 10 km that became a protected area (Reserve Speciale) in 1986: an 80-ha gallery forest and a 520-ha xerophytic spiny forest. The region has a diversity of habitats and a very diverse and highly endemic flora and fauna, including four species of lemurs found in or near the reserve. The ringtailed lemur (Lemur catta) and Verreaux’s sifaka (Propithecus verreauxi) have been the subject of our long-term research. In this chapter we highlight some of the results of this research. Our multidisciplinary studies illustrate the feasibility of collecting long-term data on careers of individual animals and of obtaining large samples on numerous animals, across numerous social groups, in relatively isolated breeding populations. Thus, we can provide insights into many of the demographic, socioecological, anthropogenic, and epidemiological factors that shape the local ringtailed lemur and sifaka population. Here we summarize how ringtailed lemur demographic structure is affected by climatic perturbations (drought); how aspects of general health (parasite loads and dental health) are directly related to habitat, dietary, and anthropogenic factors; how tight birth seasonality in sifaka can elicit stress responses in males associated with increased male aggression, group takeovers, and infanticide risk; how life history schedules are related to evolutionary responses to extreme climatic fluctuations; and how directional selection among sifaka males leads to longer, stronger legs, but not to increase in male body mass relative to females.

The emergence of longevous populations

Significance Public interest in social and economic equality is burgeoning. We examine a related phenomenon, lifespan equality, using data from charismatic primate populations and diverse human populations. Our study reveals three key findings. First, lifespan equality rises in lockstep with life expectancy, across primate species separated by millions of years of evolution and over hundreds of years of human social progress. Second, industrial humans differ more from nonindustrial humans in these measures than nonindustrial humans do from other primates. Third, in spite of the astonishing progress humans have made in lengthening the lifespan, a male disadvantage in lifespan measures has remained substantial—a result that will resonate with enduring public interest in male–female differences in many facets of life. The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Female and male life tables for seven wild primate species

We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica; baboon (Papio cynocephalus) and blue monkey (Cercopithecus mitis) in Kenya; chimpanzee (Pan troglodytes) in Tanzania; and gorilla (Gorilla beringei) in Rwanda. Using one-year age-class intervals, we computed point estimates of age-specific survival for both sexes. In all species, our survival estimates for the dispersing sex are affected by heavy censoring. We also calculated reproductive value, life expectancy, and mortality hazards for females. We used bootstrapping to place confidence intervals on life-table summary metrics (R0, the net reproductive rate; λ, the population growth rate; and G, the generation time). These data have high potential for reuse; they derive from continuous population monitoring of long-lived organisms and will be invaluable for addressing questions about comparative demography, primate conservation and human evolution.

Paternal Care in Propithecus verreauxi coquereli

Alloparental behavior is documented for several anthropoid primates, but few researchers have investigated the extent or variability of such behavior in prosimians. We report results from a study of male-infant interactions in 2 groups of Coquerel’s sifaka (Propithecus verreauxi coquereli) at the Duke University Primate Center (DUPC). Both groups contained 1 adult pair, 2 juveniles, and a newborn. The adult males exhibited paternal behavior toward their offspring in the form of grooming and holding the infant, though males differed in the amount of time they spent engaged in these activities. Group differences in the proximity maintained between the infants’ parents suggest that the relationship between adult males and females may help account for the variation. The presence of juveniles appeared to diminish paternal behavior in the group exhibiting a higher overall rate of male-infant interaction.

Lemurs Making a Living in Unpredictable Environments

The lemurs of Madagascar have been the subject of field research for over five decades, the resulting considerable body of literature providing important new insights into the ecology, behavior, and evolution of Madagascar’s unique primate radiation. Lemurs: Ecology and Adaptation, edited by Lisa Gould and Michelle Sauther, represents a compilation of 20 chapters by 29 contributors who have conducted field work in Madagascar. The editors’ rationale for publishing this volume is to provide a single source for disseminating the results of new research on lemurs spanning the last fifteen years, including summaries of long-term research on well-known taxa as well as newly studied species. They believe these contributions will provide a better understanding of mammalian adaptations to harsh environments, many of which arise from anthropogenic causes. The book is divided into four sections covering lemur origins and ecology, the evolution of lemur traits, ecology and adaptation, and lemur adaptations to changing environments. Section One sets the evolutionary stage for the sections that follow, its three chapters providing reviews of lemur origins (Tattersall), the history of ecological studies of lemurs (Jolly and Sussman), and the ecology of recently extinct lemurs (Godfrey et al.). Malagasy lemurs are, not surprisingly, monophyletic, most likely derived, according to Tattersall, from a single forest canopy dwelling African strepsirrhine ancestor that colonized Madagascar during the early Tertiary. We learn from Godfrey et al.’s fascinating contribution that the ecological profiles of Madagascar’s primate communities were substantially different in the past than they are in the present, and that the special adaptations that are present in extinct forms most likely reflect the species’ energy conservation lifestyles. Jolly and Sussman catapult us into the present with a comprehensive and engagingly written review of the history of ecological studies of Malagasy lemurs, supplemented with a detailed summary of all lemur research conducted since the 1950s. Section Two is composed of three review and two data chapters focusing on the evolution of lemur traits. Cuozzo and Yamashita review recent data on the impact of ecology on teeth in extant lemurs and conclude (unsurprisingly) that tooth morphology is related to physical properties of food, yielding optimal designs for processing specific food. Curtis explores the proximate J Mammal Evol (2008) 15:215–217 DOI 10.1007/s10914-008-9073-y