Dental senescence in a long-lived primate links infant survival to rainfall

Abstract

Primates tend to be long-lived, and, except for humans, most primate females are able to reproduce into old age. Although aging in most mammals is accompanied by dental senescence due to advanced wear, primates have low-crowned teeth that wear down before old age. Because tooth wear alters crown features gradually, testing whether early dental senescence causes reproductive senescence has been difficult. To identify whether and when low-crowned teeth compromise reproductive success, we used a 20-year field study of Propithecus edwardsi, a rainforest lemur from Madagascar with a maximum lifespan of >27 years. We analyzed tooth wear in three dimensions with dental topographic analysis by using Geographical Information Systems (GIS) technology. We report that tooth wear exposes compensatory shearing blades that maintain dental function for 18 years. Beyond this age, female fertility remains high; however infants survive only if lactation seasons have elevated rainfall. Therefore, low-crowned teeth accommodate wear to a point, after which reproductive success closely tracks environmental fluctuations. These results suggest a tooth wear-determined, but rainfall-mediated, onset of reproductive senescence. Additionally, our study indicates that even subtle changes in climate may affect reproductive success of rainforest species.lemur ͉ longevity ͉ wild population ͉ Ranomafana Park ͉ life history

Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar

“…Population growth rates of the closely related Verreaux's sifaka (Propithecus verrauxi), inhabiting southern dry forests, have been found to be most sensitive to drought conditions (Lawler et al, 2009). In RNP, King et al (2005) demonstrated that aging P. edwardsi females with senescent teeth had little success raising young especially in years with dry lactation seasons. Drought during lactation in the present study was negatively associated with first year survival but with relatively low weighted importance (Table 2), and was not associated with fecundity overall, suggesting that at current levels, it is unlikely to have much effect on population dynamics.…”

“…We had expected that drought would be one of the most important factors likely to threaten P. edwardsi populations in the face of climate variability (Wright, 2006;Dunham et al, 2008) based on suggestions of prior studies (Gould et al, 1999;Richard et al, 2000;King et al, 2005). Population growth rates of the closely related Verreaux's sifaka (Propithecus verrauxi), inhabiting southern dry forests, have been found to be most sensitive to drought conditions (Lawler et al, 2009).…”

“…Like most lemurs, P. edwardsi are sexually monomorphic in size (Dunham & Rudolf, 2009) and a previous study of the same population (Dunham et al, 2008) showed no significant difference in survival to 1 year of age when offspring of known sex were compared (Student's t-test, t 5 0.20, df 5 17, P 5 0.842). We focused on fecundity because population growth rate of this species has been shown to be sensitive to changes in this parameter (Dunham et al, 2008) and it may be the most sensitive parameter to environmental change (King et al, 2005). Fecundity and first year survival were arcsine square root transformed for normality.…”

Reproductive fitness and tooth wear: Milking as much as possible out of dental topographic analysis

“…Although this result may at first seem counterintuitive, King et al (1) point out that fertility is not necessarily the best measure of reproductive success. In this case, mortality rates are higher for infants of dentally senescent mothers.…”

“…A similar study of stomach contents in Milne Edwards' sifakas, along with analyses of milk production and nutrient content, would go a long way toward confirming links between dental morphology, lactation, and environment. Nevertheless, by combining long-term field studies with dental topographic analyses, King et al (1) offer an exciting new way of thinking about occlusal morphology, reproductive fitness, and natural selection. This research challenges the rest of us, raising the bar not only on analyses of tooth wear but also on all studies of adaptive form and function.…”