Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size

Abstract

The multiple skeletal components of the skull originate asynchronously and their developmental schedule varies across amniotes. Here we present the embryonic ossification sequence of 134 species, covering all major groups of mammals and their close relatives. This comprehensive data set allows reconstruction of the heterochronic and modular evolution of the skull and the condition of the last common ancestor of mammals. We show that the mode of ossification (dermal or endochondral) unites bones into integrated evolutionary modules of heterochronic changes and imposes evolutionary constraints on cranial heterochrony. However, some skull-roof bones, such as the supraoccipital, exhibit evolutionary degrees of freedom in these constraints. Ossification timing of the neurocranium was considerably accelerated during the origin of mammals. Furthermore, association between developmental timing of the supraoccipital and brain size was identified among amniotes. We argue that cranial heterochrony in mammals has occurred in concert with encephalization but within a conserved modular organization.

Figure 1. Reconstructed ossification sequence of the hypothetical common ancestor of Mammalia using squared-change parsimony under a Brownian motion model.

The skull of the mammaliaform Morganucodon is used to show the adult bone topology. The skull is in lateral view and the lower jaw in lingual view. Septomaxilla, coronoid and articular (malleus) were not applicable or studied herein. Abbreviations: as, alisphenoid (epipterygoid); bo, basioccipital; bs, basisphenoid; de, dentary; eo, exoccipital; et, ectotympanic (angular); fr, frontal; go, goniale (prearticular); ju, jugal; la, lacrimal; mx, maxilla; na, nasal; os, orbitosphenoid; pa, parietal; pal, palatine; pe, petrosal; pg, pterygoid; pm, premaxilla, so, supraoccipital; sq, squamosal. This material is reproduced and modified with permission of John Wiley & Sons, Inc. Copyright 1981 (John Wiley & Sons, Inc).

Figure 2. Heterochronic shifts in the onset of skull bone ossification recovered by the Parsimov-based genetic inference (PGi) analysis in amniotes.

Significant shifts detected in derived nodes compared with ancestral nodes are summarized. A, acceleration; D, delay. Numbers in the tree represent the detected cranial elements.

Figure 3. Relation between encephalization quotient (EQ) and supraoccipital ossification timing.

Supraoccipital timing was obtained by calculating the relative score of the supraoccipital within all cranial bones. Significant negative correlation was found between supraoccipital timing and EQ (r= −0.65, n=48, P<0.0001).

Figure 4. Phylogenetic independent contrasts between EQ and supraoccipital timing.

Supraoccipital timing is negatively correlated with the EQ (r= −0.60, n=47, P<0.0001).

Figure 5. Reconstructed heterochronic shifts of supraoccipital developmental timing.

Values were reconstructed using squared-change parsimony under a Brownian motion model.

Figure 6. Variation of developmental timing of all bones.

Results are shown for highly resolved species with more than four ranks. (a) Boxplot comparison of the range of variation of relative timing of cranial bones (dermal bones in red and endochondral bones in blue). The 25–75th percentiles are shown using a box. The whiskers show the top of the box up to the largest data point <1.5 times the box height from the box. Values further than 1.5 times the box height from the box are shown as circles, and those further than three times are shown as stars. Relative ossification timing is indicated to be significantly different between pooled dermal bones and pooled endochondral bones (Mann–Whitney U-test, P<0.00001). (b) Neighbour-joining cluster analysis of developmental timing. Bootstrap values were obtained through 10,000 permutations. Cranial bones form two clusters such as a dermal bone cluster and an endochondral bone cluster. (c) Topology of dermal and endochondral bones (prenatal Bos taurus). Abbreviations: as, alisphenoid; bo, basioccipital; bs, basisphenoid; de, dentary; eo, exoccipital; et, ectotympanic; fr, frontal; go, goniale; ju, jugal; la, lacrimal; mx, maxilla; na, nasal; os, orbitosphenoid; pa, parietal; pg, pterygoid; pm, premaxilla, so, supraoccipital; sq, squamosal.