Craniofacial skeletal response to encephalization: How do we know what we think we know?

Abstract

Dramatic changes in cranial capacity have characterized human evolution. Important evolutionary hypotheses, such as the spatial packing hypothesis, assert that increases in relative brain size (encephalization) have caused alterations to the modern human skull, resulting in a suite of traits unique among extant primates, including a domed cranial vault, highly flexed cranial base, and retracted facial skeleton. Most prior studies have used fossil or comparative primate data to establish correlations between brain size and cranial form, but the mechanistic basis for how changes in brain size impact the overall shape of the skull resulting in these cranial traits remains obscure and has only rarely been investigated critically. We argue that understanding how changes in human skull morphology could have resulted from increased encephalization requires the direct testing of hypotheses relating to interaction of embryonic development of the bones of the skull and the brain. Fossil and comparative primate data have thoroughly described the patterns of association between brain size and skull morphology. Here we suggest complementing such existing datasets with experiments focused on mechanisms responsible for producing the observed patterns to more thoroughly understand the role of encephalization in shaping the modern human skull.

Keywords: brain; cranial capacity; development; human evolution; mouse models; skull morphology.

© 2019 American Association of Physical Anthropologists.

Figures

FIGURE 1

Estimated cranial capacity across hominin species ordered by their estimated geological age. Red and blue circles: Average cranial capacity for female and male, respectively, modern Homo sapiens. Green and yellow circles: Minimum and maximum cranial capacity estimates for fossil hominins. Species showing only a green circle indicate that only a single cranial capacity estimate was available in the literature (de Sousa & Cunha, 2012; Elton, Bishop, & Wood, 2001; Holloway et al., 2004; Rightmire, 2004)

FIGURE 2

Representative hominin fossils showing the progressive intensification of neurocranial globularity, facial retraction, and cranial base flexion with increased encephalization

FIGURE 3

Cranial base angle shown on a sagittal section of 3D reconstruction of adult gorilla (left), human neonate (center), and adult human (right). Though diverse measures have been proposed to estimate cranial base angle (solid red line), we show the angle constructed using the landmarks basion, sella, and foramen caecum, with sella as the vertex of the angle (black circle), with the angle measured on the ventral side (dotted yellow line)

FIGURE 4

3D reconstruction of computed tomography images of a human neonate (left) showing positioning of cranial base synchondroses (yellow box). Illustration of a sagittal section (right) of the human cranial base showing individual bones and synchondroses

FIGURE 5

Brain development. (a) Early development of neural tube from neuroectoderm (adapted from Richtsmeier & Flaherty, 2013). (b) Morphogenesis of brain from neural tube and formation of major brain regions (adapted from Shiraishi et al., 2015). CS = Carnegie stage

FIGURE 6

3D reconstruction of computed tomography images of a newborn modern human skull indicating mode of ossification (adapted from Flaherty et al. 2016) and showing timing of mineralization of individual skull elements (see Sperber et al., 2010). B = bilateral

FIGURE 7

(a) It is commonly accepted that environmental and genetic influences contribute to the production of phenotypic variation. (b) A developmental perspective accepts the production of phenotypic variation as a higher order emergent result of genetic and environmental influences. These influences provide information that is used by cells to modify developmental pathways that affect phenotypes and life-history traits resulting in changes in our interaction with the environment, including human society. To make sense of these complex relationships, anthropologists must continue to use technologies from other disciplines and expand their collaborative efforts, forming research teams that focus on all hierarchical levels, from the molecule to populations