SCIENCE ADVANCES | RESEARCH ARTICLE ANTHROPOLOGY Copyright © 2022 The Authors, some Frontal sinuses and human evolution rights reserved; exclusive licensee American Association Antoine Balzeau1,2*, Lou Albessard-Ball1,3, Anna Maria Kubicka1,4, Andréa Filippo1, for the Advancement Amélie Beaudet5,6,7, Elena Santos8,9,10, Thibault Bienvenu11, Juan-Luis Arsuaga8, of Science. No claim to Antonis Bartsiokas12, Lee Berger13, José María Bermúdez de Castro10,14, Michel Brunet15,16, original U.S. Government Kristian J. Carlson17,18, Joan Daura19,20, Vassilis G. Gorgoulis21,22,23,24, Frederick E. Grine25, Works. Distributed Katerina Harvati26, John Hawks27, Andy Herries28,29, Jean-Jacques Hublin30,31, Jiaming Hui1, under a Creative Commons Attribution Rachel Ives32, Josephine A. Joordens33,34, Yousuke Kaifu35, Mirsini Kouloukoussa36, License 4.0 (CC BY). Baptiste Léger37, David Lordkipanidze38,39, Ann Margvelashvili38,39, Jesse Martin40, María Martinón-Torres10,14, Hila May41,42, Aurélien Mounier1,12, Anton du Plessis43, Todd Rae44, Carolin Röding45, Montserrat Sanz20,46, Patrick Semal47, Dominic Stratford48, Chris Stringer30, Mirriam Tawane49, Heiko Temming30, Evangelia Tsoukala50, João Zilhão51,52,53, Bernhard Zipfel54, Laura T. Buck55 The frontal sinuses are cavities inside the frontal bone located at the junction between the face and the cranial vault and close to the brain. Despite a long history of study, understanding of their origin and variation through evolution is limited. This work compares most hominin species’ holotypes and other key individuals with extant hominids. It provides a unique and valuable perspective of the variation in sinuses position, shape, and dimen- sions based on a simple and reproducible methodology. We also observed a covariation between the size and shape of the sinuses and the underlying frontal lobes in hominin species from at least the appearance of Homo erectus. Our results additionally undermine hypotheses stating that hominin frontal sinuses were directly affected by biomechanical constraints resulting from either chewing or adaptation to climate. Last, we demon- strate their substantial potential for discussions of the evolutionary relationships between hominin species. INTRODUCTION thermoregulatory adaptation [e.g., (17)] or that they serve to disperse Sinus presence and morphology have been used in systematics in masticatory strain [e.g., (18)]. An alternative is that sinuses have no phylogenetically disparate taxa (1, 2), and there is some evidence function at all and are evolutionary spandrels in the sense described that pneumatic variation may be diagnostic in Middle and Late by Gould and Lewontin (19). The different hominin sinus types Pleistocene hominins (3–6). Relationships between hominins re- (frontal, maxillary, sphenoidal, and ethmoidal) are not functionally main far from clear and potentially phylogenetically informative or developmentally homologous (6, 20); thus, we focus here solely characters such as frontal sinus morphology that may be useful in on the frontal sinuses. Although we do not explicitly test functional elucidating them. Among extant primates, ethmoidally derived frontal hypotheses, our results from comparisons of frontal sinus morphol- sinuses are present only in Gorilla, Pan, and Homo (7, 8), and we ogy among hominin and nonhuman primate taxa are informative have recently characterized morphology in these genera (9). Knowl- in the context of this debate. edge of the variation in size and shape of frontal pneumatization The present study aims to (i) quantify variation in frontal sinus during human evolution, however, is limited. In original specimens, shape and size for each available hominin species, using linear and pneumatization is usually only directly observable when they are volumetric measurements, and to compare these results to large sam- fragmented. In this context, most of the evidence resides in brief ples of extant hominines; and (ii) to describe and quantify patterns descriptions that appear occasionally as part of detailed presenta- of bilateral variation in the frontal sinuses to investigate the possible tions of fossil individuals. The few comparative studies of hominin relationship between sinus form and the position of the underlying frontal sinuses to date have been based on restricted samples and fo- frontal lobes of the brain (as reflected by the endocast) following cused either on comparing Homo neanderthalensis to Homo sapiens patterns suggested by our previous investigation of extant taxa (9). or on the distinctive sinuses of Middle Pleistocene Homo (3, 6, 10, 11). Our results bring original and previously unknown insights to Moreover, frontal sinus shapes show great complexity and extreme understanding the origin of hominin frontal pneumatization by high- levels of variation within and between taxa. Imaging and quantifica- lighting the phylogenetic importance of this character and its rela- tion of such variation are difficult, and most studies have therefore tionship with other aspects of the cranium. Our study also contributes focused on quantitative analysis of size. Here, we apply a simple, strongly to the characterization of hominin cranial anatomy in dif- repeatable method for quantifying and comparing sinus shape and ferent taxa. position and additionally quantify and compare frontal sinus size in a large sample of extinct hominins and extant nonhuman African apes. In addition to uncertainty regarding the taxonomic patterning RESULTS of frontal sinus variation, debate continues over their potential func- Sinus size and shape variation tion. Many varied explanations have been proposed for sinus func- Descriptive information illustrating variation in frontal sinus mor- tion (12–14), from aquatic adaptation (15) to acoustic adaptations phology between and within a total of 21 hominin species (69 fos- (16). Two hypotheses of enduring popularity are that sinuses are a sil hominin specimens) is given in the Supplementary Materials Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 1 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE (Supplementary Text and figs. S2 to S70 in frontal, lateral, and supe- robustus (DNH 155), and Paranthropus boisei (OH 5). Two Homo rior orientations) and summarized in Fig. 1. We also detail informa- individuals also plot within this variation: the Homo naledi individ- tion on the available imaging dataset and comment on preservation ual Lesedi 1 and D4500 from Dmanisi. Early Homo fossils would of the relevant anatomical area for each fossil hominin individual probably also plot in this distribution if we could measure both (table S2). Morphometric data for pneumatization of the frontal their endocranial size and the volume of their frontal sinuses. Other bone for each individual are presented in table S3, and an illustra- hominin species, with larger brains, do not follow this pattern and tion of the measurements taken is shown in Fig. 2. This detailed plot outside of this distribution. H. sapiens (that includes large sam- information is provided for future comparative purposes. ples of recent individuals and several fossil individuals with all the The relationship between the cube root of the volume of the characteristic features of our species) has a particular position in frontal sinuses and the cube root of the endocranial volume is infor- relation with restricted pneumatization compared to other species, mative regarding global variation in frontal sinus size (Fig. 3). There in terms of both the absolute extension and the proportion of un- was a significant correlation between sinus size and endocranial size pneumatized individuals. when the complete sample for Pan and Gorilla is considered [slope = A principal components analysis (PCA) of all the linear mea- 1.36, correlation coefficient (r) = 0.72, P = 10 × 10−16]. We observed surements computed on the data before adjustment for size illus- a nonsignificant relationship and large variation in sinus size inde- trates the strong influence of sinus size on distinguishing extant and pendently of endocranial size (slope = 2.17, r = 0.089, P = 0.53) fossil groups. Separation on the first axis is mainly due not only to when fossil hominins were included with nonhuman great apes. size (Fig. 4) but also to shape, particularly in the antero-posterior The variation in hominin sinus volume fell within the range of vari- and lateral dimensions, which separate out Gorilla from the other ation observed in Pan and Gorilla, with a few exceptions (Fig. 3). taxa, and in the supero-inferior dimensions, which separate out re- Broken Hill 1 is at the upper extreme of variation, such that only cent H. sapiens. Pan and fossil hominins have an intermediate posi- one Gorilla gorilla specimen has larger sinuses, while Bodo and tion on the first axis. Broken Hill 1, Petralona, and Bodo have large Petralona have the largest sinuses in the entire sample. Fossil hominins values on the first axis and are isolated on this axis. A PCA computed with small brain sizes plot within the endocranial variation observed on relative (size-adjusted) data distinguishes well on the second axis for Pan and Gorilla, which tend to show a linear relationship be- between recent/fossil H. sapiens and Pan/Gorilla, while, again, fossil tween brain volume and sinus size. This is the case for Sahelanthropus hominin species have intermediate positions (Fig. 5). tchadensis (TM 266-01-060-1), Australopithecus africanus (Sts 5 and In the analyses of both absolute and relative measurements, the early 71, StW 505), Australopithecus prometheus (StW 573), Australopithecus hominin individuals, which include Sahelanthropus, Australopithecus, garhi (Bou-VP-12/130), Australopithecus sediba (U.W. 88), Paranthropus and Paranthropus, plot together and fall between Pan and Gorilla 1 UMR 7194 Histoire Naturelle de l’Homme Préhistorique, CNRS, PaleoFED Team, Département Homme et Environnement, Muséum national d’Histoire naturelle, Paris, France. 2Department of African Zoology, Royal Museum for Central Africa, Tervuren, Belgium. 3PalaeoHub, Department of Archaeology, University of York, York, UK. 4 Department of Zoology, Poznań University of Life Sciences, Poznań, Poland. 5Department of Archaeology, University of Cambridge, Cambridge, UK. 6School of Geography, Archaeology and Environmental Studies, University of the Witwatersrand, Johannesburg, South Africa. 7Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain. 8Centro Mixto UCM-ISCIII de Evolución y Comportamiento Humanos, Departamento de Paleontología, Facultad Ciencias Geológicas, Universidad Complutense de Madrid, 28040 Madrid, Spain. 9Cátedra de Otoacústica Evolutiva y Paleoantropología (HM Hospitales - Universidad de Alcalá), Departamento de Ciencias de la Vida, Universidad de Alcalá, Alcalá de Henares, Spain. 10Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo de la Sierra de Atapuerca 3, 09002 Burgos, Spain. 11Department of Anthropology and Anthropological Museum, University of Zurich, CH-8052 Zurich, Switzerland. 12Department of History and Ethnology, Democritus University of Thrace, Komotini, Greece. 13Centre for the Exploration of the Deep Human Journey, University of the Witwatersrand, WITS, Johannesburg 2050, South Africa. 14Anthropology Department, University College London, London, UK. 15Chaire de Paléoanthropologie Humaine, Collège de France, Paris, France. 16UMR 7262 CNRS, Université de Poitiers, Poitiers, France. 17Evolutionary Studies Institute, University of the Witwatersrand, Palaeosciences Centre, Wits, Johannesburg 2050, South Africa. 18Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA 90089, USA. 19Departament d’Història i Arqueologia, Facultat de Geografia i Història, Universitat de Barcelona, c/Montalegre 6, 08001 Barcelona, Spain. 20Centro de Arqueologia da Universidade de Lisboa (UNIARQ), Faculdade de Letras de Lisboa, Universidade de Lisboa, Alameda da Universidade, 1600-214 Lisboa, Portugal. 21Department of Histology and Embryology, Medical School, National and Kapodistrian University of Athens, Athens, Greece. 22Biomedical Research Foundation of the Academy of Athens, Athens, Greece. 23Ninewells Hospital and Medical School, University of Dundee, Dundee, UK. 24Division of Cancer Sciences, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester M20 4GJ, UK. 25Departments of Anthropology and Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA. 26Senckenberg Center for Human Evolution and Paleoenvironment and Institute for Archaeological Sciences, Eberhard Karls Universität Tübingen, Rümelinstr. 23, 72070 Tübingen, Germany. 27University of Wisconsin-Madison, Madison, WI 53706, USA. 28Department of Archaeology and History, La Trobe University, Bundoora, VIC 3086, Australia. 29Palaeo-Research Institute, University of Johannesburg, Gauteng, South Africa. 30Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany. 31Chaire de Paléoanthropologie, Collège de France, 75005 Paris, France. 32Centre for Human Evolution Research, History Museum, London, UK. 33Naturalis Biodiversity Center, Leiden, Netherlands. 34Faculty of Science and Engineering, Maastricht University, Netherlands. 35The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan. 36Museum of Anthropology, Medical School, National and Kapodistrian University of Athens, Athens, Greece. 37Columbia University, 116 Street & Broadway, New York, NY 10027, USA. 38Georgian National Museum, Purtseladze Str. 3, 0105 Tbilisi, Georgia. 39 Ivane Javakhishvili Tbilisi State University, Chavchavadze Av. 1, 0179 Tbilisi, Georgia. 40Palaeoscience, Department of Archaeology and History, La Trobe University, Bundoora, VIC 3086, Australia. 41Department of Anatomy and Anthropology, Sackler Faculty of Medicine, Tel Aviv University, Post Office Box 39040, Tel Aviv 6997801, Israel. 42Shmunis Family Anthropology Institute, Dan David Center for Human Evolution and Biohistory Research, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel. 43Physics Department, Stellenbosch University, Stellenbosch, South Africa. 44Centre for Research in Evolutionary Anthropology, Department of Life Sciences, Roehampton University, Holybourne Avenue, London SW15 4JD, UK. 45Paleoanthropology, Senckenberg Centre for Human Evolution and Palaeoenvironment, Eberhard Karls University of Tübingen, Tübingen, Germany. 46Grup de Recerca del Quaternari (GRQ-SERP), Departament d’Història i Arqueologia, Universitat de Barcelona, Carrer Montalegre, 6, 08001 Barcelona, Spain. 47Royal Belgian Institute of Natural Sciences, Brussels 1000, Belgium. 48School of Geography, Archaeology and Environmental Studies, University of the Witwatersrand, WITS, Johannesburg 2050, South Africa. 49Ditsong National Museum of Natural History, Pretoria, South Africa. 50Laboratory of Geology and Palaeontology, School of Geology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece. 51UNIARQ-Centro de Arqueologia da Universidade de Lisboa, Faculdade de Letras, Universidade de Lisboa, 1600-214 Lisbon, Portugal. 52Catalan Institution for Research and Advanced Studies, 08010 Barcelona, Spain. 53 Department of History and Archaeology, University of Barcelona, 08007 Barcelona, Spain. 54Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa. 55Research Centre for Evolutionary Anthropology and Palaeoecology, School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, UK. *Corresponding author. Email: abalzeau@mnhn.fr Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 2 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE Fig. 1. Schematic diagram summarizing variation among taxa and evolutionary changes in hominin frontal sinus morphology. The diagonal line divides taxa that seem to show different constraints on sinus morphology (specimens are not shown to scale; they are globally organized chronologically from base to top). Weak constraint on sinus development from surrounding anatomical structures and large frontal superstructures providing potential space for expansion give the sinuses the opportunity to develop isometrically with endocranial size (Fig. 3) in genera Pan, Gorilla, Sahelanthropus, Australopithecus, and Paranthropus (see right). In later hominins (see left), integration between the cranium, brain, and sinuses appears to influence sinuses expansion. Within later Homo, characteristics of sinus morphol- ogy are indicated by different colored ellipses (color code corresponds to that used inFigs. 3 to 5). Our results support the existence of separate groups within Middle Pleistocene hominins. On the basis of the frontal sinuses, there appears to be an evolutionary relationship between H. neanderthalensis and one group, which may be called H. heidelbergensis, while the group containing Broken Hill 1, and so reasonably called H. rhodesiensis, has a unique morphology that supports a distinct status. Covariation between the size and shape of the sinuses on both sides and the underlying frontal lobes has existed since at least H. erectus and was present among subsequent hominin species. on the one hand and the later hominins on the other. H. naledi plots Morphometric trends between H. sapiens populations in the center of the distribution of Homo erectus for both the abso- When a linear discriminant analysis of the different geographic sam- lute and relative size analyses. H. erectus s.l. shares with H. sapiens a ples of recent H. sapiens was computed on the dataset of absolute higher degree of variation in sinus extension. The H. neanderthalensis measurements, the resulting confusion matrix showed a proportion and most European Middle Pleistocene hominin distributions over- of correctly classified individuals of 33.9%. This low level of correct lap partly in both analyses. A group composed of Broken Hill 1, classification illustrates the large variation observed within samples Bodo, and Petralona plots outside of the distribution of all other and a lack of geographic partitioning in sinus size/shape. A multi- hominin samples due to their much larger sinuses (Fig. 4). In terms variate analysis of variance, however, shows some significant differences of relative dimensions, these three fossils plot at the intersection of between pairs of samples that were investigated through additional early hominins and H. erectus because of their relatively large ante- analyses. The resulting squared Mahalanobis distances (table S5) high- ro-posterior sinus dimensions compared to other hominin species light some closer affinities and differences between groups, but there is (Fig. 5). The individual attributed to Homo antecessor plots well with- no clear geographic patterning. Last, we tested for a potential cor- in the distribution of other Middle Pleistocene hominins for both relation between sinus dimensions and geography. To do so, a PCA absolute and relative analyses. TD6-15 has absolutely smaller sinuses, was calculated on sinus dimensions of the different samples of ex- possibly relating to its individual age, than the H. neanderthalensis tant H. sapiens. PC1 accounts for 91.95% of the variation in this individuals (table S3, Fig. 4, and fig. S34) but falls within the extant human sample. Spatial autocorrelation was not observed in H. neanderthalensis range of variation for the relative data (Fig. 5). the dataset (Mantel test, P = 0.1662), which means that the frontal Fossil and recent H. sapiens have relatively small sinuses of distinc- sinus measurements in one population are not more similar to those tively great height (supero-inferior dimensions). These morphometric of geographic neighbors than they are to groups at a greater distance. results complement the visible variation in sinus shape (Supplemen- We also calculated a generalized linear model (table S6) to see whether tary Text and table S4). individuals from various regions differed in the measurements of Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 3 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE Fig. 2. Visualization and quantification of the frontal sinuses. The skull of the type specimen of H. neanderthalensis, Feldhofer 1, in anterior (A), superior (B), and de- tailed views (C). Bone is rendered transparent, and sinuses are shown as a virtual solid in magenta. Dimensions of the frontal sinuses are measured as 2D projections in different orientations and are shown as follows: maximal lateral extension (W), maximal height (H), and maximal length of the left and right frontal sinuses [anterior length (AL): ALl and ALr] measured from the most medial and inferior point of the sinus to the more distant point of the extension of the sinus vertically and laterally measured in anterior view; maximal medio-lateral extension of the left and right sinus [superior length (SL): SLl and SLr] measured in superior view; length from the most anteriorly protruding point of the sinus to the most posterior point in a horizontal direction (AP) and length from the most anterior point to the maximal supero-posterior extension of the sinuses (AP2) measured in left lateral view (see also fig. S1). their frontal sinuses. These results illustrate that, although the Mantel was necessary to consider specimens individually due to poor pres- tests showed that the dimensions of the frontal sinuses are not spa- ervation in many individuals precluding sample-wide analysis. In tially autocorrelated, they differed significantly between geographic Sts 5 and StW 505 (A. africanus), there appears to be a left frontal regions (see P values in table S6). petalia of the brain associated with a smaller sinus on the left side. In U.W. 88 (A. sediba), a right frontal petalia is associated with a Bilateral variation in sinus and brain anatomy larger left sinus. We observe a tendency among our sample of Asian Within the recent H. sapiens sample, among 345 individuals, 41 do not H. erectus for the left sinus to be larger than the right sinus, and have sinuses (aplasia), 24 have no sinus on the right side, and 9 have most of these fossils show a right frontal petalia. The exception is no sinus on the left side. There is a tendency toward greater sinus ex- Sangiran 17, which has a left frontal petalia. In Middle Pleistocene tension toward the left, resulting in significant directional asymmetry hominins, the left sinus tends to be larger than the right sinus, and (DA). The mean values right minus left (R-L) for anterior length a right frontal petalia is observed in all individuals that allow evalu- (AL) and superior length (SL) are −2.23 and −2.25 mm (t = −4.3113, ation of this trait. In H. neanderthalensis, there is no clear asymmetric P = 2.2 × 10−05; t = −3.806, P = 0.0002, respectively). This shows that tendency in the sinuses at the scale of the sample, which might result frontal sinuses in H. sapiens tend to be larger on the left side, as mean from the incomplete preservation in many individuals. Nevertheless, values (R-L) for AL and SL are negative and significantly different a right frontal petalia is the most common pattern and appears to from zero. Asymmetrical sinus development in recent H. sapiens has be paired with qualitatively greater extension of the left sinuses been shown to be associated with right petalias (frontal lobe expan- (R petalia and L > R sinus) in La Ferrassie 1, Gibraltar 1, Krapina 3, sion in the brain) (9). On the left side, it appears that sinus develop- and Spy 1. ment takes advantage of the greater space available, resulting in greater pneumatization. In Pan and Gorilla, no DA was detected for all the dimensions of the frontal sinuses (9), while petalias in these DISCUSSION taxa do show some degree of asymmetry (21). Frontal bone pneumatization and phylogenetic implications To identify potential relationships between sinus and cranial or With regard to the relationship between sinus size and endocranial brain morphology in fossil hominin taxa, we investigated several size, early hominins, including Sahelanthropus and various species features at the individual level among our sample, including bilateral of Australopithecus and Paranthropus, plot comfortably within the variation in sinus dimensions (relative to their preservation), the range of variation observed for Pan and Gorilla and at some dis- shape of the supraorbital torus (as directly observed for each indi- tance from the distribution of Homo individuals (Fig. 3). This pat- vidual), and the position of the underlying frontal lobes of the brain tern is maintained in multivariate analyses of sinus dimensions as reflected by the endocranial cast (including the petalia, i.e., the (Figs. 4 and 5). The underlying frontal lobes do not appear to influ- relative extension of respectively the right and left frontal poles). It ence sinus shape and expansion in Pan, Gorilla, and early hominins, Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 4 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE Fig. 3. Bivariate plot of the cube root of the volume of the frontal sinuses rel- ative to the cube root of the endocranial volume. Individual volume data (both in centimeters) in Pan and Gorilla (red: P. paniscus; dark orange: P. troglodytes; light Fig. 4. PCA of absolute measurements of frontal pneumatization in all directions. orange: G. gorilla) and fossils hominins (purple: Sahelanthropus, Australopithecus, Red: P. paniscus; dark orange: P. troglodytes; light orange: G. gorilla; small pink dots: and Paranthropus; gray: H. naledi; green: H. erectus s.l.; light blue: H. heidelbergensis; extant H. sapiens; purple: Sahelanthropus, Australopithecus, and Paranthropus; light green: H. rhodesiensis; dark blue: H. neanderthalensis; pink: fossil H. sapiens); gray: H. naledi; dark green: H. erectus s.l.; light blue: H. heidelbergensis; light green: the pink lines show the variation and the mean for recent H. sapiens. The black line H. rhodesiensis; dark blue: H. neanderthalensis; large pink dots: fossil H. sapiens. H, shows the regression of both variables in Pan and Gorilla (slope = 1.36, r = 0.72, height of sinuses; W, width of sinuses; 2AL, combined medio-lateral extension of P = 10 × 10−16). Labels for fossil hominins are as follows: TM 266-01-060-01 (Toumaï), sinuses in anterior view; 2AP, combined anterior projection of sinuses; 2SL, com- To; Sts 5, S5; Stw 505, S505; Sts 71, S71; Stw 573, S573; UW 88-50, U88; BOU-VP- bined medio-lateral extension of sinuses in superior view (the lines represent the 12/130, BOU; SK 48, S48; DNH 155, D155; OH 5, O5; Stw 53, S53; KNM-ER 3883, ER; direction and the loadings of these measurements along the two components; see OH 9, O9; D2280, D1; D2282, D2; D3444, D3; D4500, D4; Trinil 2, T; Sambungmacan 4, Fig. 1 for the visualization of these measurements). Labels for fossil hominins are as S4; Sangiran 17, S17; Skull IX, SIX; Ngandong 1, N1; Ngandong 7, N7; Ngandong 12, follows: TM 266-01-060-01 (Toumaï), To; Sts 5, S5; Stw 505, S505; Sts 71, S71; Stw N12; Ngawi 1, Nw1; Lesedi 1, Les; La Ferrassie 1, LF; La Quina H5, LQ; Guattari, Gu; 573, S573; UW 88-50, U88; BOU-VP-12/130, BOU; SK 48, S48; DNH 155, D155; OH 5, Forbes’ Quarry 1, Gi; Krapina 3, K3; Krapina 6, K6; La Chapelle aux Saints, LCP; Spy 1, O5; Stw 53, S53; KNM-ER 3883, ER; OH 9, O9; D2280, D1; D2282, D2; D3444, SI; Spy 10, SX; Feldhofer, F; Amud, Am; Tabun C1, Tc1; Aroeira, Ar; HK 87, H87; D3; D4500, D4; Trinil 2, T; Sambungmacan 4, S4; Sangiran 17, S17; Skull IX, SIX; H1024, H24; Sima de los Huesos Skull 5, Sh5; SHS12, Sh12; SHS13, Sh13; SHS17, Ngandong 1, N1; Ngandong 7, N7; Ngandong 12, N12; Ngawi 1, Nw1; Lesedi 1, Les; Sh17; Ceprano, C; Petralona, P; Broken Hill 1, BH; Bodo, B; Zuttiyeh, Z; Steinheim, S; La Ferrassie 1, LF; La Quina H5, LQ; Guattari, Gu; Forbes’ Quarry 1, Gi; Krapina 3, Jebel Irhoud 1, JI; LH 18, LH; Qafzeh 9, Q9; Cro-Magnon 1, C1; Cro-Magnon 2, C2; K3; Krapina 6, K6; La Chapelle aux Saints, LCP; Spy 1, SI; Spy 10, SX; Feldhofer, F; Cro-Magnon 3, C3; Pataud, Pa. Amud, Am; Apidima 2, Ap2; Tabun C1, Tc1; TD6-15, TD (yellow dot); Aroeira, Ar; HK 87, H87; H1024, H24; Sima de los Huesos Skull 5, Sh5; SHS12, Sh12; SHS13, Sh13; SHS17, Sh17; Ceprano, C; Petralona, P; Broken Hill 1, BH; Bodo, B; Zuttiyeh, Z; Steinheim, S; Jebel Irhoud 1, JI; LH 18, LH; Qafzeh 9, Q9; Cro-Magnon 1, C1; Cro-Magnon 2, C2; while the large frontal superstructures in these taxa give the sinuses Cro-Magnon 3, C3; Pataud, Pa. the opportunity to develop isometrically relative to brain size, in contrast to the condition observed among Homo species. This mor- phology, shared not only between Pan and Gorilla (9) but also with that frontal pneumatization develops in Homo species in relation to Sahelanthropus, Australopithecus, and Paranthropus, could be seen new and variable constraints related to factors such as the integra- as a primitive trait in contrast with the different conditions observed tion between the vault and the upper face, brain, and frontal sinuses. in Homo individuals. Nevertheless, with the potential exception of These groups of Homo share a reduced antero-posterior extension Stw 53, which has been tentatively attributed to Homo gautengensis of the sinuses compared to early hominins and show variation in (22) but more conventionally to Australopithecus sp. (23) or Homo the extension of the sinuses in the lateral and vertical directions, cf. habilis (24, 25) and shows the primitive frontal sinus size and depending on taxon (table S4). These differences may be an indirect shape, we feel that this finding cannot be used to clarify the taxo- consequence of the differences in cranial morphology between taxa, nomic attribution of disputed early hominin fossils. With regard to as already suggested [e.g., (6, 10)], and of different evolutionary tra- Stw 53, its primitive sinus morphology may support its exclusion jectories. However, that does not prevent their potential utility in from the genus Homo. taxonomic analyses. In contrast to the relative homogeneity of sinus morphology in Despite its relatively small brain size, H. naledi does not follow nonhuman apes and early hominins, we observe differences in frontal the pattern of frontal pneumatization seen in other small-brained sinus size and shape between H. erectus s.l., H. neanderthalensis, Mid- hominins but is in the center of the range of variation observed for dle Pleistocene hominins, and fossil H. sapiens. Our results suggest H. erectus s.l. both for multivariate analyses of absolute and relative Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 5 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE craniodental anatomy in H. erectus as a species have been noted [e.g. (28, 29)] and have caused some to argue that the taxon should be divided (30, 31). However, many see this level of variation as commensurate with what should be expected in a long-lived, geo- graphically widespread primate species (28, 32). High levels of variation in sinus size and shape are visible among Middle Pleistocene hominins, particularly because of the huge pneumatization of Bodo, Broken Hill 1, and Petralona. These indi- viduals are unique in terms of the size and shape of their sinuses, which might support their grouping in a separate taxon that could be called Homo rhodesiensis due to the presence of the holotype of the species in the group (i.e., Broken Hill 1). Regarding the debated taxonomic position of Zuttiyeh [(33) versus (34)], the individuals’ frontal pneumatization shares more affinities with H. neanderthalensis than with H. erectus s.l. The other European Middle Pleistocene spec- imens (to the exclusion of Broken Hill 1, Bodo, and Petralona, if grouped into H. rhodesiensis) exhibit a coherent morphological pattern of frontal pneumatization, which differs from the other groups. For this reason, these fossils are grouped here into Homo heidelbergensis for ease of discussion (but note that not all authors of this paper agree on the use of H. heidelbergensis for all specimens within this group). In terms of absolute data, these individuals form a group Fig. 5. PCA of relative measurements of frontal pneumatization in all directions. close to H. neanderthalensis except for Sima de los Huesos 13 and Red: P. paniscus; dark orange: P. troglodytes; light orange: G. gorilla; small pink dots: 17, in which the sinuses are smaller, and Steinheim, which plots extant H. sapiens; purple: Sahelanthropus, Australopithecus, and Paranthropus; gray: H. naledi; dark green: H. erectus s.l.; light blue: H. heidelbergensis; light green: with H. erectus. The morphology of the frontal pneumatization of H. rhodesiensis; dark blue: H. neanderthalensis; large pink dots: H. sapiens. Hr, rela- Steinheim may nevertheless reflect taphonomic alteration. When tive height of sinuses; Wr, relative width of sinuses; 2ALr, relative combined medio-­ relative dimensions are considered, the H. heidelbergensis fossils are lateral extension of sinuses in anterior view; 2APr, relative combined anterior slightly further outside the range of H. neanderthalensis. projection of sinuses; 2SLr, relative combined medio-lateral extension of sinuses in A greater degree of variation is observed in earlier European fos- superior view (the lines represent the direction and the loadings of these measure- sils, but they also share clear affinities in sinus shape with the most ments along the two components; see Fig. 1 for the visualization of these measure- recent H. neanderthalensis, which exhibit reduced variation in sinus ments; the cube root of the volume of the pneumatization was used for trait size shape and size compared to other fossil populations. The specimens correction). Labels for fossil hominins are as follows: TM 266-01-060-01 (Toumaï), from Sima de los Huesos slightly expand the observed variation in To; Sts 5, S5; Stw 505, S505; Sts 71, S71; Stw 573, S573; UW 88-50, U88; BOU-VP- the H. neanderthalensis sample if included therein. H. neanderthalensis 12/130, BOU; SK 48, S48; DNH 155, D155; OH 5, O5; Stw 53, S53; KNM-ER 3883, ER; OH 9, O9; D2280, D1; D2282, D2; D3444, D3; D4500, D4; Trinil 2, T; Sambungmacan do not have absolutely or relatively larger sinuses compared to other 4, S4; Sangiran 17, S17; Skull IX, SIX; Ngandong 1, N1; Ngandong 7, N7; Ngandong hominins (6, 10, 35). These observations on frontal sinuses are con- 12, N12; Ngawi 1, Nw1; Lesedi 1, Les; La Ferrassie 1, LF; La Quina H5, LQ; Guattari, sistent with a potential phylogenetic relationship between at least some Gu; Forbes’ Quarry 1, Gi; Krapina 3, K3; Krapina 6, K6; La Chapelle aux Saints, LCP; fossils named here H. heidelbergensis and H. neanderthalensis, as sug- Spy 1, SI; Spy 10, SX; Feldhofer, F; Amud, Am; Apidima 2, Ap2; Tabun C1, Tc1; TD6- gested by craniofacial morphological evidence from the Sima de los 15, TD (yellow dot); Aroeira, Ar; HK 87, H87; H1024, H24; Sima de los Huesos Skull 5, Huesos, Steinheim, and Ehringsdorf individuals [e.g., (5, 30, 36, 37)] Sh5; SHS12, Sh12; SHS13, Sh13; SHS17, Sh17; Ceprano, C; Petralona, P; Broken Hill and by genetic data from the Sima de los Huesos hominins (38). 1, BH; Bodo, B; Zuttiyeh, Z; Steinheim, S; Jebel Irhoud 1, JI; LH 18, LH; Qafzeh 9, Q9; Other members of the group described here as H. heidelbergensis Cro-Magnon 1, C1; Cro-Magnon 2, C2; Cro-Magnon 3, C3; Pataud, Pa. may show different taxonomic affinities. Analyses of temporal bone pneumatization have also shown very low levels of morphological data. This is a previously unknown and important observation for variation in H. neanderthalensis (39). This is interesting in the con- this species and supports its inclusion in the genus Homo notwith- text of ancient DNA studies, which have demonstrated low levels of standing many primitive aspects of its morphology (26). genetic diversity and a high frequency of inbreeding within later Both H. erectus s.l. and H. sapiens show relatively great variation representatives of H. neanderthalensis (38, 40). in the size and shape of the frontal sinuses (table S4), including a sizeable proportion of aplasia. The Zhoukoudian, Ngandong, and Causes and modalities of expression of the frontal sinuses Sambungmacan individuals tend to have small sinuses, and several Our results illustrate various patterns of sinus variation in Gorilla, exhibit aplasia (tables S2 and S3). Sinuses are larger in the more Pan, and hominin species. We see different sinus morphologies be- ancient Indonesian and African H. erectus individuals. The five tween taxa likely undergoing relatively similar masticatory strain Dmanisi individuals constitute an interesting illustration of the level regimes, such as H. erectus s.l. and Middle Pleistocene hominins of sinus morphology variation that can be observed in H. erectus s.l. (41, 42). On the basis of these observations and previous evidence They show a very high degree of intraspecific sinus morphology (41, 42), it is very unlikely that sinus size and shape are driven by variation, although they come from a unique stratigraphic layer masticatory strains in hominins. from the same site. This is congruent with the elevated craniofacial Our results, along with multiple strands of evidence in the liter- variability observed in this sample (27). High levels of variation in ature (6, 10, 35), demonstrate that H. neanderthalensis individuals Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 6 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE are not hyperpneumatized compared to H. sapiens, H. erectus, or fossil preservation and relatively low resolution for imaging data- other hominin samples in terms of absolute or relative frontal pneu- sets are problematic for paleoanthropological research. Data access matization. In addition, there is no clear support for a functional or is another issue. Fortunately, we had here access to a unique data- a climatic origin of H. neanderthalensis pneumatization when all of base to study the variation and evolution of the hominin anatomy, the evidence (43), including observed variation among hominins, is yet there are still taxa that we were unable to access. The sample for considered. On the basis of this multiple evidence, we, therefore, pro- this study is more complete and diverse, in terms of hominin spe- pose that the long-standing hypothesis that the frontal sinuses of cies and fossil individuals included, than any previous study on pa- H. neanderthalensis are an adaptation to cold climate [e.g., (17, 44, 45)], ranasal pneumatization. The internal preservation of the crania and should be definitively rejected. the capacity of the imaging data to allow visualization of the fea- Moreover, our results obtained from large, diverse samples of tures studied have to be considered, nevertheless. Our simple and H. sapiens (Supplementary Text and tables S5 and S6) show that the pragmatic protocol allows for a large, precise, and detailed study of dimensions of the sinuses are not spatially autocorrelated, despite this complex fossil record. In this context, we revise previous in- significant differences between geographic regions. In other words, complete or erroneous characterizations of sinus morphology for no direct link is observed between geographic origin and the size some fossil individuals or species and obtain original information and shape of frontal sinuses, i.e., individuals from colder climates on the majority of the material (see Supplementary Text). are not characterized by significantly larger/smaller frontal sinuses We propose a simple, repeatable methodology for the anatomi- than populations from warmer areas. The observed differences within cal description and quantification of sinus size and shape, as well as the analyzed sample appear to be related to other factors besides a global comparative morphometric and anatomic framework for climate. We propose then that climate does not seem to directly ex- nearly all the identified hominin species. We hope that this will en- plain the development of frontal sinuses in our species. It is never- courage authors of future descriptions of key hominin skulls to re- theless likely that sinus shape and variation in living populations port detailed information about the morphology and dimensions of around the world may reflect some aspects of the recent history of the sinuses. This does not prevent researchers from doing additional our species including migrations, genetic drift, and local adapta- comparative analyses of their individuals but provides the paleo- tions. Whether these factors exert selective pressures on the sinuses anthropological community with basic knowledge of a potentially themselves or indirectly via their effects on craniofacial morpholo- important area of anatomy in fossil hominins. gy remains to be determined. On the basis of the available evidence, we conclude that large frontal superstructures induce weak constraints related to the posi- Does frontal lobe shape influence sinus shape? tion of the face and the brain and give the sinuses the opportunity A more anterior, lateral extension of the right frontal lobe of the to expand allometrically in all directions into the available space brain, as reflected by the endocranial cast, compared to the contra- in the genera Gorilla, Pan, Sahelanthropus, Australopithecus, and lateral side is a general pattern in hominins that becomes consistent Paranthropus. In later hominins, new and variable constraints re- in H. erectus, H. heidelbergensis, H. neanderthalensis (46, 47), and lated to developmental integration between the cranium, brain, and H. sapiens. This asymmetry is a well-known feature of H. sapiens, frontal sinuses as well as the timing of growth and development of all which has been described in the neuroscientific literature (48, 49, 50). these structures result in limitations in the opportunistic expansion Our observations of fossil taxa (above and as detailed in the Supple- of the sinuses into the osseous structures of the frontal bone. This mentary Materials) support the suggestion that covariation between different condition results in a lower antero-posterior extension of the size and shape of the sinuses on both sides and the underlying the sinuses compared to early hominins and Pan/Gorilla. However, frontal lobes (9) was present in hominin species from at least the differences in sinus shape and size are also observed among later appearance of H. erectus. Last, a greater extension of the frontal Homo species, and these may have some implications for phyloge- sinuses into the larger space resulting from a contralateral petalia sug- netic discussions and open original perspectives for specific studies gests that sinus development is at least, in part, opportunistic (10). to better interpret the origin of these different patterns (e.g., to inves- tigate the role of the face). Future research on extant species should A new perspective on frontal sinuses and human evolution compare the shape and size of the skull, the face, and the base to- This research opens original perspectives for the study of frontal gether with the observed variations for frontal sinuses, but applica- sinuses. A limiting factor in this analysis of complex internal anatom- tion to the fossil record will be, in essence, difficult. Concerning the ical traits during human evolution is the available information for the causes and modalities of the expression of the sinuses, our results hominin fossil record. Moreover, the comparison of the different are in agreement with the assertion that sinus size and shape are not features of bilateral frontal sinus morphology among fossil hominins driven by adaptation to masticatory strains in hominins nor due to is complicated. Several fossils do not have fully preserved bilateral climatic adaptation. pneumatization, and taphonomic alteration may alter the shape and size of the sinuses on each side, complicating the analyses of subtle bilateral differences. The small sample size for fossil hominins also MATERIALS AND METHODS prevents large-scale analyses of directional and fluctuating asymmetry. Our materials consist of imaging datasets, including a large number This is why we have considered here several features at the individ- of fossil hominins (N = 94; table S2) that are separated into different ual level among our fossil hominin sample, including the bilateral geographic and/or chronological groups as follows (species names variation of the dimensions of the sinuses in relation to their pres- that have been proposed are also mentioned): early hominins: TM ervation, the shape of the torus, and the position of the underlying 266-01-060-1 (S. tchadensis), Taung, Sts 5, Sts 71, StW 505 (A. africanus), frontal lobes to identify potential relationships between anatomical StW 573 (A. prometheus), BOU-VP-12/130 (A. garhi), U.W. 88 features and repeated patterns among hominin samples. More generally, (A. sediba), KNM-WT 17000 (Paranthropus aethiopicus), DNH 7, Balzeau et al., Sci. Adv. 8, eabp9767 (2022) 21 October 2022 7 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE DNH 155, SK 46, SK 48 (P. robustus), and OH 5 (P. boisei); early pneumatization was used for trait size correction to obtain relative Homo: Stw 53 (H. gautengensis) and SK 847 (H. cf. habilis); H. erectus s.l.: values. Size-corrected dimensions were calculated to allow for com- KNM-ER 3883; KNM-WT 15000; OH 9 (Africa); D 2280, 2282, 2700, parisons of variation in shape. The whole dataset was used for mul- 3444, and 4500 (H. erectus/georgicus); Trinil 2; Mojokerto; Ngandong 1, tivariate analyses, including PCA (Figs. 4 and 5). We also compared 2, 7, and 12; Ngawi 1; Sangiran 17; Sambugmacan 1, 3, and 4; and the variation in size, position, and extension of, respectively, the Skull IX (South-East Asia); H. floresiensis: LB1; H. naledi: DH3 right and left frontal sinuses and the bilateral variation in the shape and Lesedi 1; H. antecessor: TD6-15; Middle Pleistocene hominins: of the frontal lobes of the brain (petalias). The anteriormost point Aroeira 3 cranium; Bilzingsleben 7573; HK75 199 and 87; Ceprano; on each side is described as the right and left frontal poles following Ehringsdorf H1024; H 1025; LH 18; Sima de los Huesos skulls 5, previous experience (9). 12, 13, 15, and 17; Steinheim; Zuttiyeh; Bodo; Broken Hill 1; and Considering statistical approaches, we used several different pro- Petralona; H. neanderthalensis: Amud C1, Apidima 2, La Chapelle cedures conducted with Past 4.05 software (54). We explored the aux Saints, Feldhofer, La Ferrassie 1, Forbes’ Quarry 1, Guattari, whole information expressed by our results, including results that Krapina 3 and 6, La Quina H5, Spy 1 and 10, and Tabun C1; H. sapiens: appear to be “nonsignificant” or “negative” and do not only refer to Jebel Irhoud 1 and 2; LH18; Qafzeh 9; Hofmeyr; Cro-Magnon 1, 2, significance thresholds, as suggested by Amrhein et al. (55). The co- and 3; Mladeč 1; Pataud; Afalou 2, 12, 13, 28, 30, and 34; and Taforalt XI efficient of variation (CV = SD/mean) was corrected for a small sam- C1, XV C4, XV C5, and XVII C1. Information about resolution, as ple size using the V* parameter, which is calculated as [(1 + 1/4 N) × well as preservation of the individuals and the pneumatization, is CV] and expressed in percentages (56, 57). Linear regressions were listed in table S2. calculated with the reduced major axis algorithm (58), which mini- The recent H. sapiens sample comprises 345 adult individuals mizes the errors in both variables (59). Figures for the PCA and linear from different geographic areas: 78 individuals from Alaska; 48 regression were computed in R (R Core Team, 2014). from Greenland; 71 from the Pacific area; 40 from Spain, 63 from Poland, 9 from China, 11 from India, 5 from Peru, 8 from Mexico, SUPPLEMENTARY MATERIALS and 12 from Liberia. Computed tomography (CT) or micro-CT was Supplementary material for this article is available at https://science.org/doi/10.1126/ obtained from various sources [for details, see (6, 36, 50, 51)]. 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