Homo Sapiens: Anatomically Modern Humans (AMH)

Results
Phylogenetic modelling
Figure 2 presents the phylo-morphospace and the computed position of the ancestral nodes of hypothesis 1 (black tree) and hypothesis 2 (grey tree) of the Homo phylogeny based on 84.6% of the total variation in the data (PC1 to PC3, Supplementary Table 3). Overall, the PCs discriminate accurately the different clades of the phylogenies used. The early Homo species (H. georgicus, H. ergaster, and H. habilis s.l.) and the Neandertals have negative values along PC1 (65.6%), contrasting with H. sapiens specimens. The associated shape deformation shows a low, elongated calvarium with a strongly projecting face for negative PC1 values, while the positive values are associated with a gracile morphology showing a high, rounded calvarium and an orthognathic face compatible with the San and Khoikhoi populations (#1 and 2). PC2 (13.2%) discriminates mainly the early Homo species, which occupy the upper left part of the chart, from modern humans and Neandertals in the lower part of the morphospace. Accordingly, PC2 negative values show a typical Neandertal shape (occipital bun, mid-facial prognathism), whereas PC2 positive values correlate with a small rounded calvarium, and a strongly-projecting face. The phenotypical variation within the modern human cluster is mostly explained by PC3 (5.8%) and follows closely the topology of hypothesis 1. The early H. sapiens group is morphologically close to the H. sapiens vLCAs and fits within the 95% confidence envelope computed around them. All sub-Saharan populations present positive values (#1 to 9), as well as the Oceanians (#10 and 11) and the North Africans (#12). The Khoisans (#1 and 2) are slightly isolated on PC1, showing the most gracile morphology, while the Pygmies (#3 and 4) have the most positive values on PC3. In the negative values of PC3, South Asians (#15) stand as intermediate between Africans-Oceanians and Eurasians, Europeans (#13 and 14) cluster with South-East Asians (#16) and East-Asians (#17 and 18), and Inuits (#19 and 20) are relatively close to North Americans (#21). The computed H. sapiens vLCAs are almost identical for both hypotheses and are more distant from the ancestral node hypothesising the common ancestry between modern humans and Neandertals than the Neandertal ancestor (Fig. 2).


Fig. 2

The differences between hypotheses 1 and 2 are subtle. However, the phylogenetic signals37,38 computed for hypothesis 1 appear stronger than the ones computed for hypothesis 2 (Supplementary Table 4). This may indicate a better fit of the phenotypic data to phylogenetic hypothesis 1, which includes an earlier wave of dispersal from Africa to Eurasia that preserves a phenotypic signal in Oceania39, supported by the similarity of Australians and Papuans with sub-Saharan Africans. The Khoisans and Pygmies branch from the main modern human populations close to the H. sapiens LCA13,40, but are anatomically derived and gracile41. Removing these two groups from the modelling (hypotheses 1b and 2b, Fig. 1) does not alter the coherence of the distribution of the main clades (early Homo, Neandertals and H. sapiens) or the topologies of both hypotheses in the phylo-morphospace (PC1 to PC3, 85.9%, Supplementary Table 5, Supplementary Fig. 2). However, hypothesis 2b (grey) generates differences impacting on most of the nodes of the tree, resulting in vLCA2b being closer to current modern humans than vLCA1b, and the Australian/Papuan phenotype requiring longer branches between ancestral nodes and terminal taxa to be fitted to the hypothesised topology. This is demonstrated by the computed phylogenetic signals for both hypotheses (Supplementary Table 4).

Morphologies of the vLCAs
The morphologies of vLCA1 and 2 are virtually the same (Fig. 3a, surface deviation <0.16 mm, Supplementary Table 6). Both are relatively gracile in comparison to LMP African fossils; vLCA1 is slightly more robust, with a more receding frontal and a more protruding occipital (Fig. 3b). As expected, the vLCAs present most of the morphological features that would be considered as specific of H. sapiens. On the calvarium, the neurocranium is rounded and globular; the frontal bone exhibits a well-developed frontal tuber42 and discontinuous supercilliary arches; the parietals show distinct parietal eminences; and the basicranium is markedly flexed. The face is retracted, showing an angulated and forward facing zygomatic43, along with a developed maxillary canine fossa with two strongly marked curves (incurvatio horizontalis and sagitallis44). Nevertheless, they also share features with more archaic phenotypes: in norma lateralis, the frontal is slightly receding, the brow-ridges are projecting frontward, and separated from the frontal squama by a slight sulcus, the face shows alveolar prognathism, the zygomatic process is aligned with the crista supramastoidea42, the mastoid processes are weakly developed, and the elongated occipital shows a degree of lambdoid protrusion, which together with a slight depression at obelion, appears like an incipient occipital bun. The last two features could recall the Neandertal morphology12. In norma frontalis, the antero-posterior border of the maxilla (incurvatio inframalaris frontalis) is weakly marked, as observed in H. heidelbergensis s.l.44, and the interorbital distance is particularly wide45. Thus, the vLCAs capture both the uniquely derived aspects of a modern human morphology, and the currently geographically dispersed retention of plesiomorphic characters among different human populations. Hypotheses 1b and 2b, computed in the absence of the Khoisans and Pygmies, generate ancestral shapes which differ only slightly from those based on the original hypotheses (Supplementary Fig. 3a and b). The maximum surface deviation between vLCA1 and 1b and vLCA2 and 2b is nevertheless larger (respectively, <1.00 mm and <2.96 mm, Supplementary Table 6). vLCA1b shows slightly more projecting brow-ridges, but a less prognathic face, while 2b is clearly less robust than vLCA2. When compared to each other the difference is larger (<3.13 mm, Supplementary Table 6) and vLCA2b presents a more gracile morphology (Supplementary Fig. 3c).


Fig. 3

Morphology of the vLCAs and of the LMP fossils. a Norma frontalis, lateralis, verticalis, occipitalis of vLCA1 when compared to vLCA2 through a surface deviation analysis. The histogram indicates the distribution of the deviation in mm between each vertex of the 3d models. b From left to right, norma frontalis and lateralis of Omo II, LH18, Florisbad, KNM-ES 11693 (the norma lateralis view is mirrored), and Irhoud 1. Source data are provided as a Source Data file

Discussion
The methodological approaches used in the present study have inherent uncertainties—biases from using different means and/or operators46,47,48 to obtain 3D data, number of variables versus the number of specimens, sliding of semilandmarks49,50,51, and sampling error to obtain mean population shapes52. To minimise this, the data were collected by a single operator; we reduced the number of variables by using PCs53 instead of aligned 3D coordinates throughout the study, and test models were run on non-slid semilandmarks, as well as subsamples of landmarks and semilandmarks (Supplementary Figs. 7–10). Supplementary Fig. 8 shows that the number of landmarks and the use of slid semilandmarks50 do not impact the reliability of the results. While sample size remains limited to the available fossil sample, sampling error can be assessed in the bgPCA analyses where specimens were analysed individually (Figs. 4 and 5, Supplementary Data 1–4). Finally, the modelling approach used here computes ancestral shapes which are weighted averages derived from the terminal taxa of a phylogenetic hypothesis54 of given topology using a Brownian motion model for evolution that mostly estimates drift. Those ancestral estimations are not intended to accurately represent evolution, but to act as tools to study the African LMP hominin fossil record in order to bring new insights into the origin of H. sapiens.

Our findings show that, first, the phenotypic data presented in this study relate closely to the genetic history39,55 of the considered populations. This is illustrated by the phylo-morphospace based on mean population shape data (Fig. 2), but also by the distribution of individual specimens’ shapes (Figs. 4 and 5). In addition, hypothesis 1, which takes into account an early out-of-Africa which preserves a phenotypic signal among the people of Sahul39, and hypothesis 2, which follows a more classic out-of-Africa event55, led to the computation of ancestral morphologies which are virtually undistinguishable (Fig. 3a, Supplementary Table 6). Yet, the topology of the phylogenetic tree of hypothesis 1 fits more closely the phenotypic variation of the data, as exemplified by the phylogenetic signal computed for the different phylogenies (Supplementary Table 4). The exclusion of the Khoisans and Pygmies has little impact on the first hypothesis, as the phenotype of vLCA1 and 1b remains comparable (Supplementary Fig. 3). Hypothesis 2 is more affected by this change, resulting in a very gracile morphotype (Supplementary Fig. 3) and lower values for the phylogenetic signal metrics (Supplementary Table 4). Therefore, the scenario simulated in hypothesis 1 appears to be slightly better supported by the phenotypic data presented here, which is congruent with recent genomic results14,39.

Second, the vLCAs’ morphologies are gracile and modern. The derived cranial features of H. sapiens are fully displayed in the vLCAs—a domed neurocranium, a reduced face and a marked basicranial flexion17, and only partly balanced by more archaic features (i.e., projecting brow-ridges, marked alveolar prognathism, weakly developed mastoid processes, elongated occipital bone, weakly marked incurvatio inframalaris frontalis, and wide interorbital distance; see refs. 12,42,44,45). One explanation for this gracile morphology can be found in the structure of the phylogenetic hypotheses. Under a Brownian Motion model of evolution, branch length contributes significantly to the ancestral reconstruction at the nodes54. Terminal taxa with long branch length will contribute more to the ancestral estimation. In the present hypotheses, the strongest influence on the ancestral reconstruction should be the Khoisans and Pygmies and, to a lesser extent, early H. sapiens. The Khoisans and Pygmies branch out very early from the H. sapiens stem lineage13,40, which may give an ‘archaic’ weight to their particularly gracile morphologies41. The derived morphologies of these populations, partly due to adaptation to the environment56, should be different from their ancestors’ phenotypes. The shape of the vLCAs may hence be influenced by this Khoisan/Pygmy morphological pattern by overestimating the antiquity of this gracile phenotype. This effect may only be partly balanced by the comparatively large and robust individuals (Qafzeh 6 and 9, and Skhūl V) of the early H. sapiens terminal taxon, since they are chronologically older than extant human populations and have a consequently shorter branch length (i.e., ~100 ka19,57). However, the early H. sapiens taxon plots within the 95% confidence envelope of the vLCAs in the phylo-morphospaces (Fig. 2 and Supplementary Fig. 2). In addition, the divergent morphologies (Supplementary Figs. 2 and 3) estimated from the b hypotheses reinforce this idea: the least plausible phylogeny (hypothesis 2b) yields the least plausible ancestral estimation for modern humans (vLCA2b). Thus, the gracile morphology of the computed vLCAs, while influenced by the theoretical framework of the modelling approach used here, appears to be more than just an artefact of the derivation of the ancestral morphologies from the extant descendants.

Despite the aforementioned uncertainties, and given the phenotypic affinities displayed by the LMP African hominins, a palaeoanthropological interpretation of those results is possible. The rapid fixation of the derived cranial traits shared by all recent H. sapiens with variable expression of robusticity traits58 could explain the phenotypes of the vLCAs. This could possibly have occurred through a process of localised drift during the very late Middle Pleistocene leading to population structuring16. The African LMP fossil mosaic morphologies combine archaic and modern characters, and the first occurrence of a full modern morphotype is not documented before Omo I (195 ka) and BOU-VP16/1 specimen from Herto (160 ka). None of the other LMP fossils shows the combined expression of modern human derived traits, while the computed vLCAs are modern humans and the universal cranial characters shared by all members of the species are present. This could support a rapid appearance of H. sapiens, consistent with the punctuated equilibrium theory59, however there is no evidence for a long and stable period of stasis in the Middle Pleistocene fossil record. On the contrary, current evidence suggests a dynamic biogeographic period driven by pronounced shifts in aridity and temperature60, during which drift and selection would have acted to create diversity at population and potentially species levels.

This scenario is consistent with the high level of phenotypic diversity in the LMP African hominin record. The results presented here highlight this diversity and allow to hypothesise the existence of different LMP morphotypes in Africa reflecting a structured population history (Fig. 4b). Three broad morphological patterns may be identified in the LMP fossil record: one represented by the Eastern African fossil LH18, the African LMP fossil sharing the least affinities with modern humans and the computed vLCAs (although some distortions61 on the calvarium may partly explain these phenotypic affinities); another exemplified by the North African fossil Irhoud 1, whose morphology is intermediate between modern humans and the Neandertals; and a possible third morph, represented by the South African fossil of Florisbad, and, to a lesser extent by the East African fossils KNM-ES 11693 and Omo II. Those three specimens present the shortest Euclidean distances to modern humans in all four analyses when the vLCAs are not taken into consideration (Supplementary Data 1–4). Indeed, the second shortest Euclidean distances observed is between Florisbad and early H. sapiens, between KNM-ES 11963 and the San, and between Omo II and early H. sapiens, and for analysis D with Alaskan Inuit (Supplementary Data 1–4). On the other hand, shortest Euclidean distance between Irhoud 1 and other groups is always to the South European Neandertals, except for analysis B where it is with early H. sapiens. Analysis B focuses mostly on the face which is where modern human-like traits have been identified in Irhoud 118. Finally, Florisbad is the LMP fossil most similar to the vLCAs, as exemplified by the Euclidean (Supplementary Data 1, 3, and 4) and Procrustes distances (Supplementary Figs. 4 and 5), and by the presence of a well-defined canine fossa, a fully formed tuber frontale and weakly projecting brow-ridges (Fig. 3b).

These results resonate with the age of the South African H. naledi remains4, a small-brained hominin with an unusual mosaic of ancient and modern traits, dated to the beginning of the LMP (i.e., 335–236 ka32). Both the discovery of an LMP ‘archaic’ looking Homo species and the results of the present study underline the complexity of the morphological variation within the genus Homo during the African LMP. As well as a high degree of population structure within the sapiens evolving lineage as suggested by our analyses, this complexity may encompass the presence of different Homo lineages in Africa. While some populations descending from an African H. heidelbergensis lineage may have coalesced to form H. sapiens following the African Multiregionalism hypothesis9, it is likely that some LMP African fossils were not associated with any population ancestral to H. sapiens. We should thus expect to find LMP fossils in Africa that were members of chronologically and geographically overlapping side branches of the Pleistocene human evolution tree, as the H. naledi remains seem to be4, reflecting different time-depths of lineage formation and extent of adaptive differences.

The eventual loss of these side branches could be the result of the cumulative effect of differential resilience to both climate change and inter-group competition. While the LMP fossil and archaeological record is at present insufficient to build a coherent model of diachronic change in population distributions, it could suggest a multi-phase16 process for the evolution of modern humans and their diversity. After the origin of the species in the late Middle Pleistocene, a second phase characterised by the successful expansion of modern human populations16 may have started as early as 194 ka3 but is clearly established by 130 ka, as documented by the increase in number of archaeological sites62, and the presence of a modern human population in the Levant3,43. The H. sapiens fossils from East Asia63, whose lower chronological boundary may extend to 120 ka64, may have been part of this earlier expansion phase. Genomic analysis offer conflicting evidence regarding such an early expansion of modern humans in Eurasia. The reported introgression of modern human DNA into Neandertals who lived ca. 100,000 years ago in the Altai Mountains65 would suggest that African populations had indeed expanded beyond the Levant during the last interglacial, as do some of the results based on the genotypic variation of Australians and Papuans today14,39,55. The contribution of this out-of-Africa dispersal during Marine Isotope Stage (MIS) 5 to the origin of current human diversity in Eurasia remains unclear. Nevertheless, other hominin populations and species (e.g., naledi) in Africa seem to have largely disappeared by MIS5, possibly due to the harsh climatic conditions during MIS666, which may have triggered local extinction events, and to competition with expanding groups of H. sapiens during the early phases of MIS5.

Following from these results, it is possible to tentatively draw a framework for the origin of H. sapiens. The speciation process appears to have been complex, going through different phases16 that may not have contributed to the genetic and phenotypic structure of current modern human populations. A first stage of phenotypic diversification, from 350 to 200 ka, may have happened locally with different contemporary populations forming local morphs of pre-H. sapiens groups as they are represented in the LMP fossil record. This phase may have been followed by a period of fragmentation and differential expansion of populations leading to hybridisation and coalescence of groups, which could have resulted in the emergence of morphologically derived populations of anatomically modern humans between 200 to 100 ka, as exemplified by the fossils from Herto, Skhūl and Qafzeh. Nevertheless, our results suggest that it is unlikely that all LMP local populations would have contributed equally, or at all, to the lineage that gave rise to the population ancestral to H. sapiens; local extinctions and founder effects would have shaped considerably the emergence of anatomically modern humans16. The morphology of the vLCAs computed in the present study appears to be closer to this last phase (i.e., 200–100 ka) than to the former one. This may indicate that chronologically older fossils of anatomically modern H. sapiens, representing populations which outlived most of the LMP hominin groups, are yet to be found.


Nature Communicationsvolume 10, Article number: 3406 (2019)