Broca’s area, variation and taxic diversity in early Homo from Koobi Fora (Kenya)

Reviewer #1 (Public Review):

The cerebral cortex, or surface of the brain, is where humans do most of their conscious thinking. In humans, the grooves (sulci) and bumps (convolutions) have a particular pattern in a region of the frontal lobe called Broca's area, which is important for language. Specialists study features imprinted on the internal surfaces of braincases in early hominins by casting their interiors, which produces so-called endocasts. A major question about hominin brain evolution concerns when, where, and in which fossils a humanlike Broca's area first emerged, the answer to which may have implications for the emergence of language. The researchers used advanced imaging technology to study the endocast of a hominin (KNM-ER 3732) that lived about 1.9 million years ago (Ma) in Kenya to test a recently published hypothesis that Broca's remained primitive (apelike) prior to around 1.5 Ma. The results are consistent with the hypothesis and raise new questions about whether endocasts can be used to identify the genus and/or species of fossils.

Reviewer #2 (Public Review):

The authors tried to support the hypothesis that early Homo still had a primitive condition of Broca's cap (the region in fossil endocasts corresponding to Broca's area in the brain), being more similar to the condition in chimpanzees than in humans. The evidence from the described individual points to this direction but there are some flaws in the argumentation.

First, only one human and one chimpanzee were used for comparison, although we know that patterns of brain convolutions (and in addition how they leave imprints in the endocranial bones) are very variable.

Second, the evidence from this fossil specimen adds to the evidence of previously describe individuals but still not yet fully prove the hypothesis.

Third, there is a vicious circle in using primitive and derived features to define a fossil species and then using (the same or different) features to argue that one feature is primitive or derived in a given species. In this case, we expect members of early Homo to be derived compared to their predecessors of the genus Australopithecus and that's why it seems intriguing and/or surprising to argue that early Homo has primitive features. However, we should expect that there is some kind of continuum or mosaic in a time in which a genus "evolves into" another genus. This discussion requires far more discussions about the concepts we use, maybe less discussion about what is different between the two groups but more discussion about the evolutionary processes behind them.

Fourth, the data of convolutional imprints presented are rather subjective when identifying which impressions represent which brain convolutions. Not seeing an impression does not necessarily mean that the corresponding brain feature did not exist. Interestingly, the manuscript does not mention and discuss at all the frontoorbital sulcus. This is a sulcus that usually runs from the orbital surface of the frontal lobe up to divide the inferior frontal gyrus in chimpanzees, a condition totally different than in humans who do not have a frontoorbital sulcus. Could such a sulcus be identified, this would provide a far more convincing argument for a primitive condition in this specimen. In Australopithecus sediba, e.g., the condition in this region seems to be a mosaic in which some aspects of the morphology seem to be more modern while one of the sulcual impressions can well be interpreted as a short frontoorbital sulcus. For this specimen, by the way, I would come back to my third point above: some experts in the field might argue that this specimen could belong to Homo rather than Australopithecus...

According to my arguments above, I think that this manuscript might revive interesting discussions about this topic but it is not likely to settle them because the data presented are not strong enough to fully support the hypothesis.

Reviewer #3 (Public Review):

The authors provide a detailed analysis of the sulcal and sutural imprints preserved on the natural endocast and associated cranial vault fragments of the KNM-ER3732 early Homo specimen. The analyses indicate a primitive ape-like organization of this specimen's frontal cortex. Given the geological age of around 1.9 million years, this is the earliest well-documented evidence of a primitive brain organization in African Homo.

In the discussion, the authors re-assess one of the central questions regarding the evolution of early Homo: was there species diversity, and if yes, how can we ascertain it? The specimen KNM-ER1470 has assumed a central role in this debate because it purportedly shows a more advanced organization of the frontal cortex compared to other largely coeval specimens (Falk, 1983). However, as outlined in Ponce de León et al. 2021 (Supplementary Materials), the imprints on the ER1470 endocranium are unlikely to represent sulcal structures and are more likely to reflect taphonomic fracturing and distortion. Dean Falk, the author of the 1983 study, basically shares this view (personal communication). Overall, I agree with the authors that the hypothesis to be tested is the following: did early Homo populations with primitive versus derived frontal lobe organizations coexist in Africa, and did they represent distinct species?

I greatly appreciate that the authors make available the 3D surface data of this interesting endocast.

Author Response

Reviewer #1 (Public Review):

The cerebral cortex, or surface of the brain, is where humans do most of their conscious thinking. In humans, the grooves (sulci) and bumps (convolutions) have a particular pattern in a region of the frontal lobe called Broca's area, which is important for language. Specialists study features imprinted on the internal surfaces of braincases in early hominins by casting their interiors, which produces so-called endocasts. A major question about hominin brain evolution concerns when, where, and in which fossils a humanlike Broca's area first emerged, the answer to which may have implications for the emergence of language. The researchers used advanced imaging technology to study the endocast of a hominin (KNM-ER 3732) that lived about 1.9 million years ago (Ma) in Kenya to test a recently published hypothesis that Broca's remained primitive (apelike) prior to around 1.5 Ma. The results are consistent with the hypothesis and raise new questions about whether endocasts can be used to identify the genus and/or species of fossils.

We would like to thank Rev. 1 for their comments on our paper.

Reviewer #2 (Public Review):

The authors tried to support the hypothesis that early Homo still had a primitive condition of Broca's cap (the region in fossil endocasts corresponding to Broca's area in the brain), being more similar to the condition in chimpanzees than in humans. The evidence from the described individual points to this direction but there are some flaws in the argumentation.

We are grateful to Rev. 2 for their comments, although we partially agree with some of them.

First, we would like to rectify the statement of Rev. 2 that we “tried to support the hypothesis that early Homo still had a primitive condition of Broca's cap”, indeed, our aim was to test this hypothesis and not to try to validate it.

First, only one human and one chimpanzee were used for comparison, although we know that patterns of brain convolutions (and in addition how they leave imprints in the endocranial bones) are very variable.

We understand the point raised by Rev. 2 about the variation of brain convolutions in humans and chimpanzees. We used atlases published by Connolly (1950), Falk et al. (2018) and de Jager et al. (2019, 2022) to analyse the endocast of KNM-ER 3732 and compare it to the extant human and chimpanzee cerebral conditions. However, in Figure 2, for the sake of clarity only two Homo and Pan specimens were used to illustrate the comparison (as it has been done in other published papers, e.g., Carlson et al., 2011; Science, Gunz et al., 2020 Sci Adv). In the revised version, we modified the manuscript to explain further our approach (line 156) “We used brain and endocast atlases published in Connolly (1950), Falk et al. (2018) and de Jager et al. (2019, 2022; see also www.endomap.org) for comparing the pattern identified in KNM-ER 3732 to those described in extant humans and chimpanzees. To the best of our knowledge, these atlases are the most extensive atlases of extant human and chimpanzee brains/endocasts available to date and are widely used in the literature to explore variability in sulcal patterns. In Figure 2, the extant human and chimpanzee conditions are illustrated by one extant human (adult female) and one extant chimpanzee (adult female) specimens from the Pretoria Bone Collection at the University of Pretoria (South Africa) and in the Royal Museum for Central Africa in Tervuren (Belgium), respectively (Beaudet et al., 2018).”.

Second, the evidence from this fossil specimen adds to the evidence of previously describe individuals but still not yet fully prove the hypothesis.

We tempered our discussion by concluding that (line 116) “Overall, the present study not only demonstrates that Ponce de León et al.’s (2021) hypothesis of a primitive brain of early Homo cannot be rejected, but also adds information […]”.

Third, there is a vicious circle in using primitive and derived features to define a fossil species and then using (the same or different) features to argue that one feature is primitive or derived in a given species. In this case, we expect members of early Homo to be derived compared to their predecessors of the genus Australopithecus and that's why it seems intriguing and/or surprising to argue that early Homo has primitive features. However, we should expect that there is some kind of continuum or mosaic in a time in which a genus "evolves into" another genus. This discussion requires far more discussions about the concepts we use, maybe less discussion about what is different between the two groups but more discussion about the evolutionary processes behind them.

We fully agree with Rev. 2 on this aspect. We believe that identifying these differences/similarities between fossil and extant hominids constitute the first step of a better understanding of the evolutionary mechanisms. Our work suggests indeed a certain continuity between genera and raises questions on the genus concept and how to interpret the specimens currently attributed to early Homo. In the revised version of the manuscript we included a reference to this possible scenario (line 134): “[…] or to the absence of a definite threshold between the two genera based on the morphoarchitecture of their endocasts (Wood and Collard, 1999).”.

Fourth, the data of convolutional imprints presented are rather subjective when identifying which impressions represent which brain convolutions. Not seeing an impression does not necessarily mean that the corresponding brain feature did not exist. Interestingly, the manuscript does not mention and discuss at all the frontoorbital sulcus. This is a sulcus that usually runs from the orbital surface of the frontal lobe up to divide the inferior frontal gyrus in chimpanzees, a condition totally different than in humans who do not have a frontoorbital sulcus. Could such a sulcus be identified, this would provide a far more convincing argument for a primitive condition in this specimen. In Australopithecus sediba, e.g., the condition in this region seems to be a mosaic in which some aspects of the morphology seem to be more modern while one of the sulcual impressions can well be interpreted as a short frontoorbital sulcus. For this specimen, by the way, I would come back to my third point above: some experts in the field might argue that this specimen could belong to Homo rather than Australopithecus...

We agree that the presence of a fronto-orbital sulcus would be more conclusive. However, this sulcus has not been identified in KNM-ER3732 and the region in which we would expect to find it is not preserved. As demonstrated by Ponce de León et al. (2021), because of the topographic relationships between sulci (and cranial structures), it is possible to interpret imprints on endocasts and the evolutionary polarity of some traits even in the absence of landmarks such as the fronto-orbital sulcus. In Australopithecus sediba the main derived feature of the endocast corresponds to the ventrolateral bulge in the left inferior frontal gyrus, and not to the sulcal pattern itself (Carlson et al., 2011 Science). However, the discussion around the taxonomic status of this taxon confirms the urgent need for reconsidering specimens from that time period and clarifying the mosaic-like or concerted evolution of the derived Homo-like traits within our lineage. Regarding the subjective nature of this approach, we invite readers to examine the specimen on MorphoSource (https://www.morphosource.org/concern/media/000497752?locale=en) and to request access to the National Museums of Kenya to the physical or virtual specimen to falsify our hypothesis.

According to my arguments above, I think that this manuscript might revive interesting discussions about this topic but it is not likely to settle them because the data presented are not strong enough to fully support the hypothesis.

We would be more than happy to consider new/other specimens with similar chronological and geographical contexts and investigate further this hypothesis in the future.

Reviewer #3 (Public Review):

The authors provide a detailed analysis of the sulcal and sutural imprints preserved on the natural endocast and associated cranial vault fragments of the KNM-ER3732 early Homo specimen. The analyses indicate a primitive ape-like organization of this specimen's frontal cortex. Given the geological age of around 1.9 million years, this is the earliest well-documented evidence of a primitive brain organization in African Homo.

In the discussion, the authors re-assess one of the central questions regarding the evolution of early Homo: was there species diversity, and if yes, how can we ascertain it? The specimen KNM-ER1470 has assumed a central role in this debate because it purportedly shows a more advanced organization of the frontal cortex compared to other largely coeval specimens (Falk, 1983). However, as outlined in Ponce de León et al. 2021 (Supplementary Materials), the imprints on the ER1470 endocranium are unlikely to represent sulcal structures and are more likely to reflect taphonomic fracturing and distortion. Dean Falk, the author of the 1983 study, basically shares this view (personal communication). Overall, I agree with the authors that the hypothesis to be tested is the following: did early Homo populations with primitive versus derived frontal lobe organizations coexist in Africa, and did they represent distinct species?

I greatly appreciate that the authors make available the 3D surface data of this interesting endocast.

We are grateful to Rev. 3 for their comments and for contextualizing our finding. We would also like to point out that, although the 3D surface can be viewed on MorphoSource, permission from the National Museums of Kenya has to be requested for studying the specimen and getting access to the physical specimen and/or the 3D model.