Reproductive fitness and tooth wear: Milking as much as possible out of dental topographic analysis
Researchers have known for generations that mammalian tooth form reflects function. The basic idea is that natural selection favors molars that are efficient at fracturing whatever foods an animal is adapted to eat. Most studies of mammalian (and, more particularly, primate) dental functional morphology have been limited to the study of unworn teeth, although such studies beg the questions, What about worn teeth? Does natural selection act to maintain their efficiency for food breakdown? This issue of PNAS contains an innovative report by King et al. (1) that addresses this very important question.
Early work on primate teeth suggested that their molars evolved to improve mechanical efficiency for chewing (2, 3). Primates that eat hard, brittle foods tend to crush these between flat, blunt molars, whereas species that consume softer and tougher items shear and slice them between long, sharp blades (Fig. 1) (4, 5). Quantitative studies of shearing crest lengths on unworn molar teeth have confirmed these form–function relationships (6).
Effects of wear (Left) and dietary adaptation (Right) on molar occlusal topography.
More recently, workers have begun to argue that limiting studies to unworn teeth gives us an incomplete picture of the form–function relationship (7, 8). Most primate teeth, whether in the mouth or museum collection, are worn. It has been assumed that selective pressures do not relax when teeth come into occlusion and begin to wear. Therefore, teeth should be “designed” to wear in a manner that keeps them mechanically efficient. This assumption seems reasonable, but it is difficult to measure effects of tooth shape on reproductive fitness.
The study by King et al. (1) examines dental senescence, the “wearing out” or end of functional life of the teeth, in Propithecus edwardsi, a large lemur that eats leaves, flowers, and fruit. Like other recent studies (7, 9), this one suggests that primate teeth maintain aspects of functional efficiency throughout most of the wear sequence but eventually “give out” once the occlusal morphology is more or less gone. Unlike others, however, this study actually offers evidence of the effects of tooth wear on reproductive success.
King et al. (1) set out to determine whether tooth wear compromises reproductive success and, if so, at what point. Their study combines nearly two decades of direct observation on P. edwardsi in the southeastern rainforest (now Ranomafana National Park) of Madagascar with a longitudinal study of changes in dental topography for these same individuals. Infant survivorship and rainfall data are related to occlusal morphology. Results suggest that wear exposes compensatory shearing blades that maintain dental function for ≈18 years. Despite waning shear potential beyond age 18, however, females continue to produce offspring at a rate of approximately one infant every couple of years, suggesting that chewing efficiency has little effect on fertility.
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. The authors suggest that this finding may relate to effects of less efficient processing and digestion of leaves on milk production. To throw an interesting twist into the mix, they observed that infants of these older mothers do survive when lactation seasons have elevated rainfall. King et al. conclude that the relationship between dental senescence and fitness is complicated and that subtle differences in diet related to climate or environment can have important consequences for reproductive success given specific tooth shapes.
Lanyon and Sanson (10) noted for koalas that the lengths of cutting edges on molar teeth are maintained throughout initial stages of tooth wear but that chewing efficiency, as measured by chewed particle size, ultimately declines. 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.
