Diversification of the ruminant skull along an evolutionary line of least resistance

Clarifying how microevolutionary processes scale to macroevolutionary patterns is a fundamental goal in evolutionary biology, but these analyses, requiring comparative datasets of population-level variation, are limited. By analyzing a previously published dataset of 2859 ruminant crania, we find that variation within and between ruminant species is biased by a highly conserved mammalian-wide allometric pattern, CREA (craniofacial evolutionary allometry), where larger species have proportionally longer faces. Species with higher morphological integration and species more biased toward CREA have diverged farther from their ancestors, and Ruminantia as a clade diversified farther than expected in the direction of CREA. Our analyses indicate that CREA acts as an evolutionary “line of least resistance” and facilitates morphological diversification due to its alignment with the browser-grazer continuum. Together, our results demonstrate that constraints at the population level can produce highly directional patterns of phenotypic evolution at the macroevolutionary scale. Further research is needed to explore how CREA has been exploited in other mammalian clades.


Fig. S1.
Linear regression analysis of log-transformed centroid size and log-transformed body mass. Note the very strong positive correlation (R^2 = 0.921). Species farthest away from the linear regression are labeled.

Fig. S2.
Homogeneity of slopes test of interspecific allometry in the ruminant skull. Allometric trajectory differed significantly by subfamily, but in each subfamily larger species have proportionally longer faces.

Fig. S3.
PCA morphospace with the raw data (top row) and with evolutionary allometry removed (bottom row). Shape variation across the morphospaces is presented in the right column. An interactive dashboard is available to visualize these different ordinations (https://danielrhoda.shinyapps.io/Ruminant_Dashboard/).

Fig. S4.
pPCA morphospace with the raw data (top row) and with evolutionary allometry removed (bottom row). Shape variation across the morphospaces is presented in the right column. An interactive dashboard is available to visualize these different ordinations (https://danielrhoda.shinyapps.io/Ruminant_Dashboard/).

Fig. S5.
Phylogenetically-aligned components analysis morphospace with the raw data (top row) and with evolutionary allometry removed (bottom row). Shape variation across the morphospaces is presented in the right column. An interactive dashboard is available to visualize these different ordinations (https://danielrhoda.shinyapps.io/Ruminant_Dashboard/).

Fig S6.
Interspecific morphospace of Cervidae (similar to Fig 3f), without moose (genus Alces). The white arrow is evolutionary allometry, and the blue transparent points are specimens. Ellipses are 95% confidence intervals of each species. Note the congruence between allometry and PC1, and the bias of the ellipses along this axis.

Fig. S7.
Interspecific morphospace with species colored by their % grass in diet value, where exclusive grazers have 100% grass in diet. The uncolored points are species for which these data were unavailable.

Fig. S8.
Distributions of random angles (gray) of the same dimensionality of our dataset (k=75) and observed angles (red) between the direction of divergence and CREA from our empirical dataset. Note that angles here can have a maximum value of 90 degrees. Table S1. Landmark definitions of the geometric morphometrics dataset, from Haber (22). 1 Suture junction between the two frontals and the nasals; at the frontal end when there is a gap 2 Suture junction between the two frontals and the parietal; at the frontal end when there is a gap 3 Supraoccipital boss at the dorsal end of the bone 4 Anteroventral suture end of the two palate bones 5 Posteroventral suture end of the two palate bones 6 Meeting point between the two basioccipitals on the foramen magnum rim 7 Meeting point between the two occipitals on the foramen magnum rim 8 Anterior tip of the premaxilla 9 Infraorbital foramen; the most posterior points on the rim from lateral view Suture junction between the parietal, squamosal, and occipital bones 15 Suture junction between the parietal, squamosal, and alisphenoid bones 16 Meeting point between the jugal, frontal, and orbital rims on the postorbital bar 17 Meeting point between the lacrimal, frontal, and orbital rims 18 Meeting point between the lacrimal, jugal, and orbital rims 19 Anterior suture end between the lacrimal and the jugal; at the point where the suture turns dorsally 20 Posterior suture end between the maxilla and the nasal 21 Subnasal meeting point of the maxilla (sometimes premaxilla) and the nasal 22 Anterior tip of the nasal 23 Meeting point between the basioccipital and the foramen magnum condyle 24 Foramen ovale; the most posterior point on the rim 25 Posterobuccal edge of the third molar alveoli; meeting point between the alveoli and the tooth