Unexpectedly rapid evolution of mandibular shape in hominins

Abstract

Members of the hominins - namely the so-called 'australopiths' and the species of the genus Homo - are known to possess short and deep mandibles and relatively small incisors and canines. It is commonly assumed that this suite of traits evolved in early members of the clade in response to changing environmental conditions and increased consumption of though food items. With the emergence of Homo, the functional meaning of mandible shape variation is thought to have been weakened by technological advancements and (later) by the control over fire. In contrast to this expectation, we found that mandible shape evolution in hominins is exceptionally rapid as compared to any other primate clade, and that the direction and rate of shape change (from the ape ancestor) are no different between the australopiths and Homo. We deem several factors including the loss of honing complex, canine reduction, and the acquisition of different diets may have concurred in producing such surprisingly high evolutionary rates. This study reveals the evolution of mandibular shape in hominins has strong morpho-functional and ecological significance attached.

Figure 1

The major axes of mandibular shape variation in primates, retrieved from GMM. Homo and the australopiths almost exclusively occupy the upper left quadrant of the plot (purple circle). At the two extremes of both axes we reported the shape deformation associated to these axes, overimposed on the primate consensus shape (in red) and a continuous colour scale representing the mandibular areas or more intense deformation, from areas where the mandible widens compared to the consensus (in red) to areas where it compresses (in blue). The image was generated by using the R package ggplot (http://ggplot2.org/) and our own R codes.

Figure 2

The evolutionary rates of mandible shape on the primate tree. The tree on the left reports rates computed according to phylogenetic Ridge Regression (coloured dots, scaled according to the rate value, from low = cyan, to high rates = magenta). The human clade, highlighted with a green semitransparent box, represents the only rate shift as indicated by the variable Brownian rate approach. On top right, the phylogenetic Ridge Regression rates (in absolute values) computed for the branches of the tree not belonging to the human clade (green) are contrasted to rates for the human clade (blue). On bottom right, phylogenetic Ridge Regression rates of individual branches of the human clade (in absolute value) plus the human clade sister species, the common chimpanzee, are collated in increasing rate value (blue bars), and contrasted to the average rate computed over the entire tree (the vertical red line). Bars without names correspond to internal nodes of the human clade. The image was generated by using the R package ggplot (http://ggplot2.org/) and our own R codes. Animal silhouettes were available under Public Domain license at phylopic (http://phylopic.org/), unless otherwise indicated. Specifically, clockwise starting from the bottom, Macaca (http://phylopic.org/image/eedde61f-3402-4f7c-9350-49b74f5e1dba/); Homo sapiens (http://phylopic.org/image/c089caae-43ef-4e4e-bf26-973dd4cb65c5/); Hylobates (http://phylopic.org/image/0174801d-15a6-4668-bfe0-4c421fbe51e8/); Cebus (http://phylopic.org/image/156b515d-f25c-4497-b15b-5afb832cc70c/) available for reuse under the Creative Commons Attribution 3.0 Unported (https://creativecommons.org/licenses/by/3.0/) image by Sarah Werning; Tarsius (http://phylopic.org/image/f598fb39-facf-43ea-a576-1861304b2fe4/); lemuriformes (http://phylopic.org/image/eefe8b60-9a26-46ed-a144-67f4ac885267/), available for reuse under Attribution-ShareAlike 3.0 Unported (https://creativecommons.org/licenses/by-sa/3.0/) image by Smokeybjb; Plesiadapis (http://phylopic.org/image/b6ff5568-0712-4b15-a1fd-22b289af904d/), available for reuse under Attribution-ShareAlike 3.0 Unported (https://creativecommons.org/licenses/by-sa/3.0/) image by Nobu Tamura (modified by Michael Keesey).

Figure 3

Multivariate angle comparisons among non-hominin apes, Homo species and the australopiths, assessed through multivariate angles between rate vectors. In (a) angles of Homo, australopiths, and non-hominin greater apes (Great Apes) are depicted starting from the common origin (the ancestor of all these species). The range of angles for each group is highlighted: Homo, transparent blue; Australopiths, transparent green; Great Apes, transparent orange. Vector length is proportional to actual vector size (i.e. the evolutionary rate). In (b) the same as with (a) but including lesser apes (Hylobatidae) highlighted in transparent purple. In (c) the angles in (a) are tested for significance by shuffling the rates among groups 10,000 times, real differences are indicated by the color bars. In (d) the angles in (b) are tested for significance by shuffling the rates among groups 10,000 times, real differences are indicated by color bars.