NEWS & VIEWS RESEARCH PAL A EOANTHRO PO LO GY

What teeth tell us Models based on developmental mechanisms described in mice and shared by most mammals are shown to accurately predict tooth size in extinct hominins, and can explain the small third molars in our species. See Letter p.477 A I D A G Ó M E Z- R O B L E S

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he third molars of modern humans — those often-troublesome molars we sometimes call wisdom teeth — are frequently very small or do not even develop. By contrast, the third molars of other hominin species in our evolutionary tree were huge, with chewing surfaces that were two to four times larger than those in an average modern human. This profound change in tooth proportions is usually explained by dietary and cultural changes considered to be unique to our species. But on page 477 of this issue, Evans et al.1 offer an explanation that may make us feel rather less special. The authors propose that the evolution of our small third molars may be explained by basic developmental mechanisms that we share with most mammals. In 2007, researchers proposed an inhibitorycascade model of dental development on the basis of experimental studies in mice2. According to this model, dental proportions are established by the relative amount of inhibitory and activatory molecules that are expressed as one tooth develops after another (the greater the net inhibition exerted by an earlier tooth, the smaller the size of the later-developing tooth). Since then, researchers have explored the extent to which this model can explain tooth proportions in other mammalian species. Evans and colleagues, alongside others3, have extended the application of this model to hominins. Evans et al. focused on the lower primary postcanine teeth (lower milk molars and permanent molars). Their results show that variation in tooth size and proportions follows a remarkably simple rule that differs slightly between two major hominin groups. In australo­piths, the group of African early hominins that includes, in this study, the genera Ardi­pithecus, Australopithecus and Paranthropus, teeth tend to get bigger towards the back of the primary molar row (up to the second or third permanent molar), with proportions that are constant irrespective of overall dental size. However, in the Homo genus, the proportional size of teeth varies with their overall size: smaller dentitions have disproportionately small third molars and tend to decrease in size from the first to the third molar. The beauty of this model is that these simple relationships have an astonishing predictive

power: by knowing only the size of a single tooth and the group to which it belongs — australo­pith or Homo — it is possible to infer with considerable accuracy the size of the remaining primary teeth. The model does not always correctly predict the location of the largest tooth, but predicted molar sizes are impressively close to observed values (Fig. 1). Dental anthropologists will be happy about this finding, but why should others care? Size and proportions are but one aspect of the variation in dental anatomy, which can be studied using morphometric traits (measurable size and shape) and non-metric traits (such as the presence or absence of particular cusps and crests). Together with cranial features, dental traits are the bread and butter of hominin evolutionary studies, because they are thought to contain genetically coded information from which species relationships can be reconstructed. However, it is increasingly recognized that dental anatomy can vary in complex scenarios in which natural selection m1

interacts with developmental and functional constraints4; this complexity may make teeth less useful for inferring phylogenies than we tend to recognize. For example, it is still debated whether the megadontia (extremely large dental size) observed in the genus Paranthropus is indicative of the evolutionary cohesion of this group, as is usually assumed, or whether it represents a convergent trend that was driven by similar ecological and developmental contexts5. At the other extreme of the dental-size spectrum, fossils from the Sima de los Huesos site in Atapuerca, Spain, which are dated to more than 400,000 years old and are considered to be closely related to Neanderthals6, show an extreme degree of third-molar reduction7. The small third molars of these hominins are surprising for a taxon that is ancestral to classic Neanderthals, who had larger third molars. However, Evans and colleagues’ model exactly predicts the strong third-molar reduction of Sima de los Huesos hominins as a result of their small overall postcanine dental size8 (Fig. 1). It remains to be understood why these hominins had such small teeth without an equivalent reduction of their faces and jaws. It is to be hoped that future experimental work will help to unveil models of the interaction between teeth and jaws that will explain this apparent paradox. Because of the paucity of hominin fossils, Evans and colleagues simplified their analysis by using species mean values. However, m2

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Figure 1 | Predicting molar size.  Evans et al.1 present a model that can use the measurement of a single tooth of a hominin (humans and other members of the human clade since the split from chimpanzees) to predict the sizes of its other lower primary postcanine teeth (milk and permanent molars). Depicted is a to-scale comparison of observed and predicted permanent-molar sizes in Paranthropus robustus, hominins from the Sima de los Huesos site, Neanderthals and modern humans (m1, first molar; m2, second molar; m3, third molar). Observed values are from refs 8 and 10, with updated values for Sima de los Huesos from ref. 11; predicted values were calculated from the observed m1 size using Evans and colleagues’ model (see Supplementary Spreadsheet 1). Following their conventions, red is used for australopith hominins and blue for members of the Homo genus; the largest tooth in each series is filled in black, along with all teeth that are more than 95% of its size. (Tooth drawings are of modern human molars, and not to scale with boxes.) 2 5 F E B R UA RY 2 0 1 6 | VO L 5 3 0 | N AT U R E | 4 2 5

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RESEARCH NEWS & VIEWS

Aida Gómez-Robles is in the Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington DC 20052, USA. e-mail: [email protected] 1. Evans, A. R. et al. Nature 530, 477–480 (2016). 2. Kavanagh, K. D., Evans, A. R. & Jernvall, J. Nature 449, 427–432 (2007). 3. Schroer, K. & Wood, B. J. Anat. 226, 150–162 (2015). 4. Gómez-Robles, A. & Polly, P. D. Evolution 66, 1024–1043 (2012). 5. Wood, B. & Constantino, P. Yearb. Phys. Anthropol. 50, 106–132 (2007). 6. Arsuaga, J. L. et al. Science 344, 1358–1363 (2014). 7. Gómez-Robles, A., Bermúdez de Castro, J. M., Martinón-Torres, M., Prado-Simón, L. & Arsuaga, J. L. J. Hum. Evol. 82, 34–50 (2015). 8. Bermúdez de Castro, J. M. & Nicolas, M. E. Am. J. Phys. Anthropol. 96, 335–356 (1995). 9. Young, N. M., Winslow, B., Takkellapati, S. & Kavanagh, K. Nature Commun. 6, 6690 (2015). 10. Wood, B. A. & Abbott, S. A. J. Anat. 136, 197–219 (1983). 11. Martinón-Torres, M., Bermúdez de Castro, J. M., Gómez-Robles, A., Prado-Simón, L. & Arsuaga, J. L. J. Hum. Evol. 62, 7–58 (2012).

C L I M ATE SC I E NCE

Hidden trends in the ocean carbon sink Simulations of the flux of atmospheric carbon dioxide into the ocean show that changes in flux associated with human activities are currently masked by natural climate variations, but will be evident in the near future. See Letter p.469 TAT I A N A I LY I N A

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he world ocean has absorbed about one-third of the carbon released by humans1, and therefore has a key role in moderating climate change. Observations2 of the ocean interior confirm that increases in carbon dioxide emissions from fossil-fuel burning are accompanied by an increase in carbon content in the upper ocean. But, surprising as it may seem, McKinley et al.3 report on page 469 that, in many ocean regions, changes in the uptake of CO2 induced by human activities are currently indistinguishable from changes driven by natural climate variations. So, are anthropogenic trends in the ocean carbon sink concealed by Earth’s own variability? As atmospheric CO2 levels increase, the ocean takes up this gas at a rate proportional to the difference of the partial pressure of CO2 (a measure of CO2 concentration in a mixture of

gases) between the air and sea2. The strength of the ocean carbon sink is determined by chemical reactions in seawater, biological processes such as photosynthesis and respiration, and physical processes, including ocean circulation and vertical mixing4. But even though these key mechanisms are known, there are considerable uncertainties regarding their yearto-year (interannual) and decadal variations5. These variations are tightly linked to modes of internal variability in the climate system — such as the El Niño–Southern Oscillation (ENSO) — that have regional to worldwide effects on weather and climate, and thereby modulate air–sea CO 2 fluxes and ocean biogeochemical cycles. Advances in observations and models have shed light on how internal climate variability controls the ocean carbon sink. Modern Earthsystem models (ESMs) that were analysed in the fifth Coupled Model Intercomparison Project (CMIP5, which compared the output of

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activation and inhibition levels are expected to be individual-specific, which may result in tooth proportions that differ between individuals of the same species. It is therefore possible that the rule they describe would not be so simple had interindividual variation been included in the model. Despite this limitation, Evans and colleagues’ paper advances palaeoanthropology in three fundamental ways. First, it draws on experimental data from mice, which are the most common model organism, to explain the variation observed in the hominin fossil record. Second, it develops a rigorous quantitative framework to formally test hypotheses related to that model. And finally, it improves our understanding of the human fossil record by identifying evolutionary changes that are developmentally linked. More importantly, Evans and colleagues’ results are relevant beyond the study of fossil teeth. Many of the developmental constraints that influence dental evolution are shared by other systems formed by the repetition of serially homologous components, such as vertebrae, ribs, limbs and digits. Teeth can therefore be useful in identifying developmental mechanisms operating in these other systems9. By extension, the authors’ model has the potential to help us understand the evolution of human traits that are associated with serially homologous structures, including our upright posture (which is influenced by vertebral anatomy), bipedal locomotion (which is linked to limb anatomy) and precision grip (which depends on the anatomy of digits). As with third-molar reduction, we tend to consider these traits the result of human-specific selective pressures, but their evolution is also fundamentally channelled by general developmental rules that humans have not escaped. ■

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Figure 1 | Fluxes of carbon dioxide from the atmosphere into the ocean.  These graphs compare the temporal evolution of the mean annual flux of CO2 into the world ocean (in petagrams of carbon per year; 1 Pg is 1015 grams) predicted by different model simulations, and from observations. Although the models and observations reveal a similar trajectory for the global change of flux, the plotted values vary considerably because of uncertainties in models and gaps in observations. The model predictions are from the fifth Coupled Model Intercomparison Project (CMIP5; blue) and from an ensemble of 100 simulations made using the Max Planck Institute Earth System Model (MPI-ESM; red). Solid lines show the average of an ensemble of model data; shaded areas show the upper and the lower boundaries of the ensemble data. Findings based on observational data7 are in black. McKinley et al.3 report simulations suggesting that anthropogenic changes in the air–sea carbon flux are currently obscured by naturally occurring flux variations. (CO2 fluxes into the ocean in CMIP5 models and in the MPI-ESM were calculated by Hongmei Li.)

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Palaeoanthropology: What teeth tell us.

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