Changes in Human Skull Morphology Across the Agricultural Transition Are Consistent with Softer Diets in Preindustrial Farming Groups
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Changes in human skull morphology across the agricultural transition are consistent with softer diets in preindustrial farming groups David C. Katza,b,1, Mark N. Grotea, and Timothy D. Weavera aDepartment of Anthropology, University of California, Davis, CA 95616; and bDepartment of Cell Biology & Anatomy, University of Calgary, Calgary, AB T2N 4N1, Canada Edited by Clark Spencer Larsen, The Ohio State University, Columbus, OH, and approved June 19, 2017 (received for review February 14, 2017) Agricultural foods and technologies are thought to have eased the differences in mode of subsistence (22, 23). Due to the complex- mechanical demands of diet—how often or how hard one had to ities of characterizing high-dimensional phenotypes in structured chew—in human populations worldwide. Some evidence suggests samples, each observed variable (shape, diet, genetic data, or a correspondingly worldwide changes in skull shape and form across proxy for it) is typically transformed from its original units to a the agricultural transition, although these changes have proved dif- matrix of pairwise distances between populations. The correlation ficult to characterize at a global scale. Here, adapting a quantitative between shape and diet distances, after accounting for population genetics mixed model for complex phenotypes, we quantify the in- history and structure, becomes the focus of the inquiry. fluence of diet on global human skull shape and form. We detect However, the essential units of morphology are shape, form, and modest directional differences between foragers and farmers. The size, not pairwise distances. The beauty of statistical shape analysis effects are consistent with softer diets in preindustrial farming is its potential to quantify and concretely represent morphological groups and are most pronounced and reliably directional when the differences in morphological units. The loss of this potential when farming class is limited to dairying populations. Diet effect magni- evaluating directional effects (diet, climate, etc.) in distance units is tudes are relatively small, affirming the primary role of neutral evo- especially unfortunate: A distance analysis quantifies the cor- lutionary processes—genetic drift, mutation, and gene flow structured relation between morphological and diet distances, but not what by population history and migrations—in shaping diversity in the hu- the morphological response to subsistence practice looks like. It is man skull. The results also bring an additional perspective to the par- the latter objective that motivates geometric morphometrics adox of why Homo sapiens, particularly agriculturalists, appear to be (24, 25) and is central to evaluating functional and evolutionary relatively well suited to efficient (high-leverage) chewing. hypotheses. Insights at this level require methods that permit di- rect analysis of morphological observations in structured samples. Here, we provide estimates of the influence of agriculture on foragers | farmers | subsistence effects | human skull form | mastication human skull shape, form, and size at a global scale. The morpho- logical observations are three-dimensional landmark data (Fig. 1 and he emergence and spread of agriculture are among the more SI Appendix,Fig.S1).Theskeletalsample(Fig.2andSI Appendix, Tremarkable developments in the evolutionary history of Document S1) is a large collection of preindustrial forager and Homo sapiens. This change in lifeway appears to be associated farmer crania (n = 559 from 25 groups) and mandibles (n = with changes in human skull shape and form. Although global 534 from 24 groups). Although bilateral landmarks were collected cranial diversity is generally well explained by neutral evolu- for most specimens, we average the sides and evaluate hemiforms so tionary processes (1–4), early farmers tend to have a chewing that somewhat fragmentary remains can be included in the sample. architecture that is, at least in some dimensions, less massive We adapt a Bayesian, quantitative genetics mixed model for than that of their hunter-gatherer counterparts (refs. 5–20 and high-dimensional phenotypes (26) to these data. For each skeletal 21, chap. 7). Explanatory scenarios cohere around the idea that element (cranium, mandible), we fit three models, each with a softer agricultural foods reduce masticatory demands, resulting different diet predictor. The diet predictors identify whether a in less robust craniofacial skeletons and reduced and reposi- tioned chewing muscles. Significance This is the essence of the “masticatory-functional hypothesis” CarlsonandVanGerven(5)posited four decades ago to explain Agriculture changed not only human culture and lifeways, but morphological differences among a chronological series of ancient human biology as well. Previous studies indicate that softer Nubian populations—from Mesolithic hunter-gatherers to Christian agricultural diets may have resulted in a less robust craniofacial agriculturalists. Subsequent forager–farmer comparisons for Euro- morphology in early farmers. However, obtaining reliable es- pean, Asian, and American samples support a trend of craniofacial reduction with agriculture (7–19). Most of these studies sample a timates of worldwide subsistence effects has proved chal- small number of geographically local populations (but see refs. 22 lenging. Here, we quantify changes in human skull shape and and 23). Local comparisons are valuable because they often provide form across the agricultural transition at a global scale. Al- a detailed picture of the cultural, dietary, and chronological context though modest, the effects are often reliably directional and for the morphological differences between closely related groups. most pronounced in craniofacial features that are directly in- In some cases, cultural and other evidence supports a hypothesis volved in mastication. of biological continuity between the foragers and descendant farmers (5–7, 10, 12, 14, 16–19). However, with few sampled Author contributions: D.C.K., M.N.G., and T.D.W. designed research; D.C.K. performed groups, it can be difficult to separate diet effects from other research; D.C.K., M.N.G., and T.D.W. analyzed data; and D.C.K., M.N.G., and T.D.W. wrote the paper. factors differentiating the populations. Moreover, the major di- mensions of reduction can vary from study to study, and some The authors declare no conflict of interest. farmer masticatory dimensions are larger in some comparisons This article is a PNAS Direct Submission. (8–10, 18). See Commentary on page 8917. An alternative approach samples many populations, globally 1To whom correspondence should be addressed. Email: [email protected]. or regionally, to assess the extent to which deviations from a This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. population genetic, neutral model of diversification correspond to 1073/pnas.1702586114/-/DCSupplemental. 9050–9055 | PNAS | August 22, 2017 | vol. 114 | no. 34 www.pnas.org/cgi/doi/10.1073/pnas.1702586114 Downloaded by guest on September 23, 2021 estimates of shape change associated with the Milk predictor, sampled with replacement from the posterior distribution of ef- SEE COMMENTARY fects. A less spherical arrangement of vectors around a landmark implies a more reliably directional diet effect. In Fig. 3, we mag- nify displacement vectors 1.5× to focus attention on their direc- tion and directional consistency. The same results are presented without magnification in SI Appendix,Fig.S2(interactive 3D plot) and for all three diet predictors in SI Appendix, Figs. S3 and S4. To highlight the most clearly directional diet effects, we pre- sent mean contrasts for landmark subsets. Notable features dis- tinguishing the skull shapes of foragers and farmers include a smaller anterior temporalis muscle, delineated by landmarks along the superior temporal line (Fig. 4); posterior displacement of the dentition, especially in the maxillary cheek teeth (Fig. 5 and SI Appendix, Fig. S5, and in 3D in SI Appendix, Fig. S6); a vertically taller palatal vault (SI Appendix, Fig. S6); and a taller mandibular coronoid process, narrower mandibular ramus, and SI Appendix Fig. 1. Landmarks. SI Appendix, Fig. S1 provides landmark names. more projecting lower chin (Fig. 3 and , Figs. S2 and S4). Whereas greater chin projection partially reflects a differ- ence in symphyseal shape, much of the contrast appears to be — specific agricultural subsistence staple is present/regular or absent/ due to a clockwise rotation of the symphysis a superimposition rare in a population: dairy (“Milk”); maize, wheat, rice, or other effect attributable to shape differences in other parts of the cereals (“Mush”); and “Soft,” which groups together all Milk and mandible. Cranial vault landmark displacements suggest that Mush populations. Diet assignments were made based on pub- vault size is large relative to facial size in farming groups (Fig. 3 SI Appendix lished archaeological, isotopic, and enthnographic reports (SI and , Figs. S2 and S3). Appendix,DocumentS1). We focus on dairy and cereals because The association of agriculture with mandibular size reduction their association with reduced oral processing demands is rela- is supported for the Milk and Soft predictors (Table 1). Man- tively uncontroversial. All models also include fixed effects for sex dibular size reduction in dairying populations is approximately and mean annual temperature, a random effect for population two-thirds the