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

Abstract

Classic theories of ageing consider extrinsic mortality (EM) a major factor in shaping longevity and ageing, yet most studies of functional ageing focus on species with low EM. This bias may cause overestimation of the influence of senescent declines in performance over condition-dependent mortality on demographic processes across taxa. To simultaneously investigate the roles of functional senescence (FS) and intrinsic, extrinsic and condition-dependent mortality in a species with a high predation risk in nature, we compared age trajectories of body mass (BM) in wild and captive grey mouse lemurs (Microcebus murinus) using longitudinal data (853 individuals followed through adulthood). We found evidence of non-random mortality in both settings. In captivity, the oldest animals showed senescence in their ability to regain lost BM, whereas no evidence of FS was found in the wild. Overall, captive animals lived longer, but a reversed sex bias in lifespan was observed between wild and captive populations. We suggest that even moderately condition-dependent EM may lead to negligible FS in the wild. While high EM may act to reduce the average lifespan, this evolutionary process may be counteracted by the increased fitness of the long-lived, high-quality individuals.

Age, state, environment, and season dependence of senescence in body mass

“…In spring, a decrease in body mass of old females was exhibited at lower elevation (down‐valley). The age‐dependent decrease is in line with predictions from classical senescence theories (Medawar, 1952; Williams, 1957) and concurs with other studies that found body mass senescence in mammals (Beirne et al., 2015; Hämäläinen et al., 2014; Nussey et al., 2011; Tafani et al., 2013; Weladji et al., 2010). Indeed, age‐dependent body mass senescence has previously been found in a closely related species, the Alpine marmot (Tafani et al., 2013).…”

“…However, in late summer, state‐dependent effects were expressed as a terminal decrease in mass over the last year of life, again only in females living at lower elevation. This result is consistent with most other recent studies on body mass senescence, which also reported terminal effects (Beirne et al., 2015; Douhard et al., 2017; Hämäläinen et al., 2014; Hammers et al., 2012; Nussey et al., 2011; Tafani et al., 2013). While a variety of factors could potentially lead to terminal decreases, it is commonly suggested that they indicate terminal illness, causing a sudden collapse in condition prior to death (Coulson & Fairweather, 2001).…”

“…However, contrary to predictions, and similar to age‐dependent effects, we primarily found state‐dependent effects in females living in the lower elevation environment. A few previous studies have also found greater intensity and earlier onset of age‐dependent senescence under more favorable versus less favorable conditions (Douhard et al., 2017; Hämäläinen et al., 2014). In those cases, selective disappearance appeared to be a critical factor.…”

“…Environmental conditions comprise factors like food abundance (Descamps et al., 2008), population density (Nussey et al., 2007), and seasonality (Hämäläinen et al., 2015), although the latter is rarely investigated. In general, few studies have explicitly tested for environmental effects on senescence trajectories, and even fewer have considered how different environmental conditions affect both onset and rate of senescence (but see, e.g., Beirne, Delahay, & Young, 2015; Hämäläinen et al., 2014). …”

Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar

“…are the smallest extant primates. Their average life span in the wild is 2-3 years, although some gray mouse lemurs (M. murinus) may live for 10 years or more (Hämäläinen et al, 2014). Mouse lemurs usually produce one litter per year (Eberle and Kappeler, 2006).…”