A simple rule governs the evolution and development of hominin tooth size

Abstract

The variation in molar tooth size in humans and our closest relatives (hominins) has strongly influenced our view of human evolution. The reduction in overall size and disproportionate decrease in third molar size have been noted for over a century, and have been attributed to reduced selection for large dentitions owing to changes in diet or the acquisition of cooking1,2. The systematic pattern of size variation along the tooth row has been described as a ‘morphogenetic gradient’ in mammal, and more specifically hominin, teeth since Butler3 and Dahlberg4. However, the underlying controls of tooth size have not been well understood, with hypotheses ranging from morphogenetic fields3 to the clone theory5. In this study we address the following question: are there rules that govern how hominin tooth size evolves? Here we propose that the inhibitory cascade, an activator–inhibitor mechanism that affects relative tooth size in mammals6, produces the default pattern of tooth sizes for all lower primary postcanine teeth (deciduous premolars and permanent molars) in hominins. This configuration is also equivalent to a morphogenetic gradient, finally pointing to a mechanism that can generate this gradient. The pattern of tooth size remains constant with absolute size in australopiths (including Ardipithecus, Australopithecus and Paranthropus). However, in species of Homo, including modern humans, there is a tight link between tooth proportions and absolute size such that a single developmental parameter can explain both the relative and absolute sizes of primary postcanine teeth. On the basis of the relationship of inhibitory cascade patterning with size, we can use the size at one tooth position to predict the sizes of the remaining four primary postcanine teeth in the row for hominins. Our study provides a development-based expectation to examine the evolution of the unique proportions of human teeth.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: All hominins show the inhibitory cascade pattern for dp3–dp4–m1 triplet, but species of Homo show greater reduction in size of posterior molars.
Figure 2: Prediction surfaces for hominin tooth sizes based on inhibitory cascade and scaling of inhibitory cascade reversal with m1 size.
Figure 3: Hominin prediction plot for primary postcanine rows.
Figure 4: Phylogenetic distribution of tooth sizes and proportions in hominins shows an origin of the Homo pattern shortly after the origin of the genus.

References

  1. 1

    Brace, C. L. Environment, tooth form, and size in the Pleistocene. J. Dent. Res. 46, 809–816 (1967)

  2. 2

    Bermúdez de Castro, J. M. & Nicolas, M. E. Posterior dental size reduction in hominids: the Atapuerca evidence. Am. J. Phys. Anthropol. 96, 335–356 (1995)

  3. 3

    Butler, P. M. Studies of the mammalian dentition. Differentiation of the post-canine dentition. Proc. R. Soc. Lond. B 109, 1–36 (1939)

  4. 4

    Dahlberg, A. A. The changing dentition of man. J. Am. Dent. Assoc. 32, 676–690 (1945)

  5. 5

    Osborn, J. W. in Development, Function and Evolution of Teeth (eds P.M. Butler & K.A. Joysey ) 171–201 (Academic, 1978)

  6. 6

    Kavanagh, K. D., Evans, A. R. & Jernvall, J. Predicting evolutionary patterns of mammalian teeth from development. Nature 449, 427–432 (2007)

  7. 7

    Butler, P. M. Studies of the mammalian dentition: I. The teeth of Centetes ecaudatus and its allies. Proc. R. Soc. Lond. B 107, 103–132 (1937)

  8. 8

    Owen, R. Odontography (Hippolyte Bailliere, 1840–1845)

  9. 9

    Townsend, G. C. & Brown, T. Morphogenetic fields within the dentition. Aust. Orthod. J. 7, 3–12 (1981)

  10. 10

    Polly, P. D. Evolutionary biology: development with a bite. Nature 449, 413–415 (2007)

  11. 11

    Renvoisé, E. et al. Evolution of mammal tooth patterns: new insights from a developmental prediction model. Evolution 63, 1327–1340 (2009)

  12. 12

    Wilson, L. A. B., Madden, R. H., Kay, R. F. & Sanchez-Villagra, M. R. Testing a developmental model in the fossil record: molar proportions in South American ungulates. Paleobiology 38, 308–321 (2012)

  13. 13

    Bernal, V., Gonzalez, P. N. & Ivan Perez, S. Developmental processes, evolvability, and dental diversification of New World monkeys. Evol. Biol. 40, 532–541 (2013)

  14. 14

    Halliday, T. J. D. & Goswami, A. Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms. BMC Evol. Biol. 13, 79 (2013)

  15. 15

    Schroer, K. & Wood, B. Modeling the dental development of fossil hominins through the inhibitory cascade. J. Anat. 226, 150–162 (2015)

  16. 16

    Wood, B. & Collard, M. The human genus. Science 284, 65–71 (1999)

  17. 17

    Haile-Selassie, Y. et al. New species from Ethiopia further expands Middle Pliocene hominin diversity. Nature 521, 483–488 (2015)

  18. 18

    Garn, S. M., Lewis, A. B. & Kerewsky, R. S. Molar size sequences and fossil taxonomy. Science 142, 1060 (1963)

  19. 19

    Kieser, J. A. & Groeneveld, H. T. The assessment of fluctuating odontometric asymmetry from incomplete hominid fossil data. Anthropol. Anz. 44, 175–182 (1986)

  20. 20

    Kegley, A. D. T. & Hemingway, J. in Voyages in Science: Essays by South African Anatomists in Honour of Phillip V. Tobias’ 80th birthday (eds G. Strkalj, N. Pather, & B. Kramer ) 35–49 (Content Solutions, 2005)

  21. 21

    Young, N. M., Winslow, B., Takkellapati, S. & Kavanagh, K. Shared rules of development predict patterns of evolution in vertebrate segmentation. Nature Commun . 6, 6690 (2015)

  22. 22

    Selmer-Olsen, R. An odontometrical study on the Norwegian Lapps. Skrift Norske Vidensk-Akademi 3, 1–167 (1949)

  23. 23

    Wolpoff, M. H. Metric Trends in Hominid Dental Evolution. Case Western Reserve University Studies in Anthropology 2 (Case Western Reserve Univ. Press, 1971)

  24. 24

    Lucas, P. W. Dental Functional Morphology (Cambridge Univ. Press, 2004)

  25. 25

    Greaves, W. S. The jaw lever system in ungulates: a new model. J. Zool. 184, 271–285 (1978)

  26. 26

    Spencer, M. A. Force production in the primate masticatory system: electromyographic tests of biomechanical hypotheses. J. Hum. Evol. 34, 25–54 (1998)

  27. 27

    Lucas, L. Variation in Dental Morphology and Bite Force along the Tooth Row in Anthropoids. PhD thesis, Arizona State Univ. (2012)

  28. 28

    Dembo, M., Matzke, N. J., Mooers, A. O. & Collard, M. Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships. Proc. R. Soc. B 282, http://dx.doi.org/10.1098/rspb.2015.0943 (2015)

  29. 29

    Kieser, J. A. Human Adult Odontometrics (Cambridge Univ. Press, 1990)

  30. 30

    Johanson, D. C. Some metric aspects of the permanent and deciduous dentition of the pygmy chimpanzee (Pan paniscus). Am. J. Phys. Anthropol. 41, 39–48 (1974)

  31. 31

    R Development Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2015)

Download references

Acknowledgements

This contribution is dedicated to the late Professor Percy Butler, the inspiration for much of this work and discoverer of the morphogenetic gradient in teeth, who unfortunately did not see this work completed. We thank M. Fortelius, G. Evans, A.-L. Khoo, F. Grine, P. Trusler, J. Adams, J. Clutterbuck, L. Chieu, D. Hocking, M. McCurry, Q. Nasrullah, T. Park and the Evans EvoMorph Laboratory for discussions and criticism of the manuscript. Thanks to M. Collard for supplementary information on the hominin phylogeny. We thank the Powell-Cotton Museum (M. Harman), American Museum of Natural History, Cleveland Museum of Natural History (L. Jellema), Museum of Comparative Zoology (J. Chupasko), Royal Belgian Institute of Natural Sciences (G. Lenglet), Royal Museum for Central Africa (E. Gilissen and W. Wendelen), National Museum of Natural History (USA), The Bavarian State Collection of Zoology (M. Hiermeier and C. Lang) and Anthropological Institute and Museum (Switzerland) (M. Ponce de León and C. Zollikofer) for access to great ape material. For access to computed tomography scans of fossil hominin material we thank the following individuals and institutions: National Museums of Kenya (E. Mbua), Ditsong National Museum of Natural History (S. Potze), University of Witwatersrand (C. Menter and B. Zipfel), Senckenberg Natural History Museum (F. Schrenk and O. Kullmer) and the Royal Belgian Institute of Natural Sciences (M. Toussaint). This study was made possible by use of material from the Burlington Growth Centre, Faculty of Dentistry, University of Toronto, which was supported by funds provided by grant (1) (number 605-7-299) National Health Grant (Canada), (data collection); (2) Province of Ontario Grant PR 33 (duplicating); and (3) the Varsity Fund (for housing and collection). All research protocols were reviewed and granted exemption by Arizona State University’s (ASU) Institutional Review Board and the Burlington Growth Centre, and informed consent was obtained for all human subjects. This research was financially supported by grants from the Australian Research Council Future Fellowship (A.R.E., FT130100968), Academy of Finland (J.J.), National Science Foundation (GRFP number 2011121784; K.S.P.), Max Planck Society (M.M.S.), Wenner-Gren Foundation (K.K.C.), Graduate and Professional Student Association at ASU (E.S.D., K.K.C.), and ASU Sigma XI chapter (E.S.D., K.K.C.). This research was also facilitated in part by a grant (48952) from the John Templeton Foundation (G.T.S.). The opinions expressed in this publication do not necessarily reflect the views of the John Templeton Foundation.

Author information

J.J. and A.R.E. conceived the project. A.R.E., E.S.D., K.K.C., K.S.P., S.J.K., M.M.S., G.C.T., G.T.S. and J.J. collected data. E.S.D. and K.K.C. independently validated application of the inhibitory cascade model to deciduous premolars. G.T.S. performed hominin taxonomic classification. M.M.S. conducted the computed tomography scanning and measurements. J.-J.H. and G.C.T. provided materials. A.R.E. performed the analyses. H.P.N. implemented individual-level prediction accuracy and confidence interval calculations. A.R.E. and J.J. took the lead in writing the paper with contributions from all co-authors.

Correspondence to Alistair R. Evans.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Homo species and australopiths differ in their pattern of tooth sizes, but all hominins and great apes follow the inhibitory cascade for dp3–dp4–m1 triplet.

The inhibitory cascade predicts that there is a linear relationship among three adjacent teeth. Area (in square millimetres) of each lower postcanine primary tooth. a, Mean area of each tooth for 15 hominin species. be, Red points and lines are species means. b, H. sapiens; black points and lines represent means of populations. c, Eight australopith species and (d) six fossil Homo species; black points and lines represent individual tooth rows (left and right rows of each specimen plotted separately). e, Four great ape species; black points and lines represent means of each sex. f, Two great ape species; black points and lines represent individuals, red points and lines are means for each sex. Sex and species means show clearer inhibitory cascade patterns than most individuals.

Extended Data Figure 2 Two- and three-dimensional measures of tooth size for six fossil hominin specimens.

Rectangular area (mesiodistal length × buccolingual width, MDBLArea), 3D area of the enamel–dentine junction (EDJ3DArea), cross-sectional area of the tooth at the cervix (CervixArea) and outline area of the outer enamel surface (OES2DArea) for each tooth position.

Extended Data Figure 3 Two- and three-dimensional measures of tooth size are highly correlated.

Bivariate plots for planar area (mesiodistal length × buccolingual width, MDBLArea), 3D area of the enamel–dentine junction (EDJ3DArea), cross-sectional area of the tooth at the cervix (CervixArea) and outline area of the outer enamel surface (OES2DArea). R2 shown for each plot. Blue line and shaded area, OLS regression and 95% confidence interval; red line and shaded area, loess smoothing and 95% confidence interval.

Extended Data Figure 4 The proportional size of each tooth shows a tight relationship with absolute size of the first molar, with the relationship differing between Homo species, australopiths and great apes.

Proportional size of each tooth (proportion of the largest tooth in the row) versus area of m1 (in square millimetres) for 15 hominin and 4 great ape species. Blue triangles and solid line, OLS regression for Homo species; red circles and dashed line, OLS for australopiths; yellow squares and dotted line, OLS for great apes.

Extended Data Figure 5 Tooth proportions of hominins are constrained by the inhibitory cascade and size of m1.

Three-dimensional space of tooth position (horizontal axis, numbered 1–5 for dp3–m3), area of m1 (axis into page) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, plane A is fitted to dp3–dp4–m1, and plane B to m2–m3. a, Homo species, plane A (cyan; R2 = 0.96) formula: HomoAPropMaxinRow = 0.238 × ToothPos − 0.00166 × AreaM1 + 0.441. Plane B (blue; R2 = 0.62) formula: HomoBPropMaxinRow = −0.0822 × ToothPos + 0.000690 × AreaM1 + 1.23. Thick blue line shows intersection of planes. b, Australopiths, plane A (light red; R2 = 0.93) formula: AustAPropMaxinRow = 0.0810 × ToothPos + 0.230 × AreaM1 + 2.38 × 10−6. Plane B (dark red; R2 = 0.07) formula: AustBPropMaxinRow = 0.00963 × ToothPos + 0.000168 × AreaM1 + 0.906. Thick red line shows intersection of planes. c, Great apes, plane A (yellow; R2 = 0.98) formula: ApeAPropMaxinRow = 0.268 × ToothPos − 0.0727 × AreaM1 + 0.173. plane B (light brown; R2 = 0.63) formula: ApeBPropMaxinRow = −0.0837 × ToothPos + 0.000337 × AreaM1 + 1.29. While the R2 values are substantially lower for the plane B regressions, the average deviations from plane B for Homo and australopiths are 0.026 and 0.022 respectively, which are lower than the equivalent values of 0.046 and 0.036 for plane A. Therefore, the low R2 values do not reflect the close fit of the data to the planes. d, Comparison of Homo, australopith and great ape planes shows that the corresponding planes and intersections for the first two groups diverge at smaller m1 sizes. The great ape planes fall between those of the other two groups. See Supplementary Videos 1,2,3,4 for 3D rotating graph animations.

Extended Data Figure 6 The size of the largest tooth in the row is closely related to the size of the m1 in hominins.

OLS regressions. HomoMaxAreaInRow = 1.312 × AreaM1 − 30.44, P = 0.001, R2 = 0.90; AustMaxAreaInRow = 1.298 × AreaM1 + 0.150, P = 0.0003, R2 = 0.90.

Extended Data Figure 7 Percentage error in estimates of each tooth compared with the prediction surfaces in Fig. 2.

Prediction surface is calculated so that m1 always has zero prediction error, therefore it is excluded from error calculations. a, Homo species; b, australopiths.

Extended Data Figure 8 Detailed contour plot (contour step = 5 mm2) for prediction surfaces of hominin tooth size.

Area of m1 and areas on contour in mm2. Blue contours are for Homo species, red for australopiths. From the mean size of one tooth position (for example, m1 at 125 mm2), the mean sizes of the remaining four teeth in the row can be predicted by following the tooth position vertically (orange line) to meet the contour of the measured size, then moving horizontally to the other tooth positions (cyan line and crosses) to read off the sizes according to the contours. When mean m1 size is 125 mm2, dp3, dp4, m2 and m3 are 62, 93, 130 and 199 mm2 respectively for a Homo species and 50, 88, 156 and 158 mm2 respectively for an australopith species.

Extended Data Figure 9 Slope of the inhibitory cascade in murines is weakly related to absolute size, unlike in hominins where there is a strong relationship.

a, Relative sizes of molars for the 29 species of murine rodents in ref. 6. b, Relative size of third molar to first molar (m3/m1) plotted against absolute size of first molar (in square millimetres) shows a weak relationship (cf. Extended Data Fig. 4). Blue line and shaded area, OLS regression and 95% confidence interval.

Extended Data Figure 10 Planes and surfaces for equations of tooth position T (horizontal) versus area of m1 AM1 (into page) versus proportion of area or area (vertical).

a, Regression plane A (cyan) and plane B (green) with proportion of area PropArea as calculated in equations 2 and 3 in Supplementary Information. b, Surfaces AreaAH (cyan) and AreaBH (green) as calculated in equations 11 and 12 in Supplementary Information. The two regions that represent the data are plane A or AreaAH on the left of the intersection and plane B or AreaBH on the right of the intersection of the two planes or surfaces, respectively. c, Prediction of m1 area using formulae for AreaAH (cyan) when T = 3 compared with the expected 1:1 relationship (black) using equation 11 in the Supplementary Information. If the cyan formula were standardized by the expected value (black), the standardized surface will correctly predict m1 size (equation 17 in the Supplementary Information).

Supplementary information

Supplementary Information

This file contains a Schematic Diagram of Results, Supplementary Methods, Supplementary Tables 1-10, and Supplementary References. (PDF 1294 kb)

Supplementary Data

This file calculates the mean areas of remaining four lower postcanine primary teeth in a row based on the mean size of a single tooth position. (XLSX 400 kb)

41586_2016_BFnature16972_MOESM89_ESM.mp4

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Homo species, Plane A (cyan) and Plane B (blue). See also Extended Data Fig. 5a. (MP4 2640 kb)

Tooth proportions of hominins are constrained by the inhibitory cascade and size of m1

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Homo species, Plane A (cyan) and Plane B (blue). See also Extended Data Fig. 5a. (MP4 2640 kb)

41586_2016_BFnature16972_MOESM90_ESM.mp4

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Australopiths, Plane A (light red) and Plane B (dark red). See also Extended Data Fig. 5b. (MP4 2773 kb)

Tooth proportions of hominins are constrained by the inhibitory cascade and size of m1

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Australopiths, Plane A (light red) and Plane B (dark red). See also Extended Data Fig. 5b. (MP4 2773 kb)

41586_2016_BFnature16972_MOESM91_ESM.mp4

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Great apes, Plane A (yellow) and Plane B (light brown). See also Extended Data Fig. 5c. (MP4 2604 kb)

Tooth proportions of hominins are constrained by the inhibitory cascade and size of m1

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). The proportional sizes of all teeth lie on two planes in 3D space. For all groups, Plane A is fit to dp3-dp4-m1, and Plane B to m2-m3. Great apes, Plane A (yellow) and Plane B (light brown). See also Extended Data Fig. 5c. (MP4 2604 kb)

41586_2016_BFnature16972_MOESM92_ESM.mp4

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). Comparison of Homo (cyan and blue), australopith (light and dark red) and great ape (yellow and light brown) planes shows that the corresponding planes and intersections for the first two groups diverge at smaller m1 sizes. The great ape planes fall between those of the other two groups. See also Extended Data Fig. 5d. (MP4 4081 kb)

Tooth proportions of hominins are constrained by the inhibitory cascade and size of m1

3D space of tooth position (horizontal axis 1, numbered 1-5 for dp3-m3), area of m1 (horizontal axis 2) and proportion of maximum in tooth row (vertical axis). Comparison of Homo (cyan and blue), australopith (light and dark red) and great ape (yellow and light brown) planes shows that the corresponding planes and intersections for the first two groups diverge at smaller m1 sizes. The great ape planes fall between those of the other two groups. See also Extended Data Fig. 5d. (MP4 4081 kb)

41586_2016_BFnature16972_MOESM93_ESM.mp4

Tooth area (vertical axis) for each tooth position (numbered 1-5 for dp3-m3) and area of m1. Tooth areas and surface for Homo species are plotted in blue, and australopiths in red. Vertical lines connecting spheres to surface show deviation of the species means from predicted size. See also Fig. 2. (MP4 4263 kb)

Prediction surfaces for hominin tooth sizes based on inhibitory cascade and scaling of inhibitory cascade reversal with m1 size

Tooth area (vertical axis) for each tooth position (numbered 1-5 for dp3-m3) and area of m1. Tooth areas and surface for Homo species are plotted in blue, and australopiths in red. Vertical lines connecting spheres to surface show deviation of the species means from predicted size. See also Fig. 2. (MP4 4263 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Evans, A., Daly, E., Catlett, K. et al. A simple rule governs the evolution and development of hominin tooth size. Nature 530, 477–480 (2016). https://doi.org/10.1038/nature16972

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.