Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago

Abstract

Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.

Mount Pinatubo, Inflammatory Cytokines, and the Immunological Ecology of Aeta Hunter-Gatherers

“…Such data, if representative, are consistent with reports of unusually long interbirth intervals (35 months) among the Aeta (Gawlik et al 2011), but not with the correlation between higher birth orders and shorter interbirth intervals among the Agta (Goodman et al 1985). Extended nursing by older Aeta mothers could be a means of suppressing ovulation and regulating population size under unfavorable conditions (Konner and Worthman 1980) or a "terminal investment" in infants born later during the maternal life cycle (Williams 1966;Fessler et al 2005;Hoffman et al 2010). For example, the terminal children of Dobe !Kung mothers are typically weaned at 48 months, or as late as 60 months, although the average age of infant weaning is 28-35 months (Howell 2010).…”

Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate

“…[16,19,20]). In the wild, studies of FS have largely focused on long-lived, large-bodied animals that face relatively low levels of environmental hazard (ungulates [10,21], sea-birds [22], seals [23] and primates [6,24]). Because FS is more detectable when EM is low, this taxonomic bias may lead to an overestimation of the prevalence of FS compared with the influences of selective disappearance in natural populations across species.…”

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques

“…In rhesus macaques, reproductive investment peaks in young adults (6-12 years of age; Dubuc et al, 2014;Hoffman et al, 2010) therefore we predicted that younger adults would show greater oxidative damage than older adults. Among lactating females, we hypothesized that levels of oxidative damage would be negatively associated with offspring age, as the energetic costs of lactation in primates tend to be highest at the beginning of infant life (Emery Thompson et al, 2012).…”