Rules of teeth development align microevolution with macroevolution in extant and extinct primates

Nature Ecology & Evolution (2023)Cite this article

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Macroevolutionary biologists have classically rejected the notion that higher-level patterns of divergence arise through microevolutionary processes acting within populations. For morphology, this consensus partly derives from the inability of quantitative genetics models to correctly predict the behaviour of evolutionary processes at the scale of millions of years. Developmental studies (evo-devo) have been proposed to reconcile micro- and macroevolution. However, there has been little progress in establishing a formal framework to apply evo-devo models of phenotypic diversification. Here we reframe this issue by asking whether using evo-devo models to quantify biological variation can improve the explanatory power of comparative models, thus helping us bridge the gap between micro- and macroevolution. We test this prediction by evaluating the evolution of primate lower molars in a comprehensive dataset densely sampled across living and extinct taxa. Our results suggest that biologically informed morphospaces alongside quantitative genetics models allow a seamless transition between the micro- and macroscales, whereas biologically uninformed spaces do not. We show that the adaptive landscape for primate teeth is corridor like, with changes in morphology within the corridor being nearly neutral. Overall, our framework provides a basis for integrating evo-devo into the modern synthesis, allowing an operational way to evaluate the ultimate causes of macroevolution.

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All of the data analysed during this study are included in the Supplementary Data.

All of the code used for this paper is available at https://github.com/MachadoFA/PCMkappa and https://github.com/MachadoFA/PrimateTeethProject.

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We thank E. Delson and colleagues for access to the PRIMO dataset49, L. Godfrey and K. Samonds for access to their Strepsirrhine molar data48, M. J. Plavcan for providing access to a large sample of dental measurement data47, G. Burin for photographing specimens at the British Museum of Natural History, G. Garbino for measuring specimens at the Museu de Zoologia João Moojen of the Universidade Federal de Viçosa, A. Kurylyuk and R. M. Rodin for providing photographs of rare Microcebus specimens and M. Surovy for providing access to the American Museum of Natural History specimens. F.A.M., J.C.U., V.D. and A.S. were funded by NSF-DEB-1942717 to J.C.U. We thank V. Mitov for his help in making a fast version of the PCMkappa, and L. Hlusko, J. Jernvall, and D. Moen and his lab for providing feedback and suggestions that greatly improved this paper.

Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA

Fabio A. Machado

Department of Anthropology, Stony Brook University, Stony Brook, NY, USA

Carrie S. Mongle

Turkana Basin Institute, Stony Brook University, Stony Brook, NY, USA

Carrie S. Mongle

Department of the Geophysical Sciences, University of Chicago, Chicago, IL, USA

Graham Slater & Anna Wisniewski

Department of Anthropology, University of Texas at San Antonio, San Antonio, TX, USA

Anna Penna

Department of Biology, Virginia Tech, Blacksburg, VA, USA

Anna Soffin & Josef C. Uyeda

Department of Anthropology, Florida Atlantic University, Boca Raton, FL, USA

Vitor Dutra

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F.A.M., C.S.M. and J.C.U. conceptualized the project. J.C.U. gathered the necessary funds. F.A.M., C.S.M., A.P., A.S. and V.D. gathered the dataset. A.W. and G.S. conducted the phylogenetic analysis. F.A.M. performed statistical analysis and produced the first draft. F.A.M., C.S.M., A.P., A.W., G.S. and J.C.U. wrote the following versions of the draft. All authors approved the last draft.

Correspondence to Fabio A. Machado.

The authors declare no competing interests.

Nature Ecology & Evolution thanks Pauline Guenser and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The Distance-space was built on the mesiodistal length (MD, vertical) and buccolingual breadth (BL, horizontal) taken from each molar. The Area-space was built by estimating the occlusal areas of each molar as the A=MDxBL. The ICM-space was built by calculating the relative area size for m2 and m3 in relation to m1.

Negative BIC values for the Gaussian mixture models for the linear distances, areas and ICM spaces for different numbers of clusters (i). EEV- Elipsoidal model with the same shape, same volume and different orientations VEE- Elipsoidal model with the same shape, different volumes and same orientation. Higher values of negative BIC suggest the best model for each morphospace.

Regimes for different runs of the heuristic search for the Distance morphospace. Left- Best model (Search 5). Right- Model compatible with the best model for areas (Fig. 3 on the main text).

Simulated regime-specific disparities for Three-regime model on morphospace. Regimes are described on the main text and illustrated on Fig. 3.

Simulated disparity (A) and phylogenetic signal (B) assuming the best model (OU) or a brownian motion (BM) model with the same rate parameters as the best OU model. Ellipses represent the covariance matrix of the simulated tip values, and thus do not represent any evolutionary parameter (for example Sigma, H, Omega, stationary variance, etc), but the phenotypic distributions of tips. Dots are observed species averages for comparison.

Phylogenetic half life for ICM ratios (m2/m1 and m3/m1) and components of the ICM model (Activation-Inhibition gradient and deviations from the ICM). Violin plots represent the distribution of values within the 95% confidence interval for the best model.

Black lines represent the phylogeny mapped to measured trait values (black points) and golden lines and golden dots represents each trait evolutionary optimum.

Differences between the Monte Carlo sampling approach for generating covariances for areas and the analytical approximation. Values are equal to the difference in coefficient of variation between matrices. Horizontal lines within violins highlights the 95% interval for each matrix cell. The first three entries are each area variance and the latter three are the areas covariances. The subscript indicates which trait (variances) or traits (covariances) are being compared.

Supplementary Materials and Methods, Tables 1–8, references and data source references.

Distances, areas and ICM measurements for living and extinct primate species.

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Machado, F.A., Mongle, C.S., Slater, G. et al. Rules of teeth development align microevolution with macroevolution in extant and extinct primates. Nat Ecol Evol (2023). https://doi.org/10.1038/s41559-023-02167-w

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Received: 19 August 2022

Accepted: 17 July 2023

Published: 31 August 2023

DOI: https://doi.org/10.1038/s41559-023-02167-w

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