Functional insights from an exploration of the inner structure of the patella: new perspectives for the study of the hominin fossil record

Cette contribution est une courte revue littéraire sur le rôle fonctionnel de la patella chez les catarrhiniens actuels et les hominines fossiles et les questions fonctionnelles, adaptatives et évolutives concernant le registre des hominines fossiles. En effet, la patella joue un rôle clé dans l’articulation du genou, reflétant postures et modes locomoteurs. Cependant, les vestiges patellaires sont rares dans le registre des hominines fossiles et l’impact possible sur la kinésiologie du genou des différences de formes et de proportions par rapport à la condition humaine actuelle reste toujours incertain. Illustré par le premier exemple sur un échantillon d’une patella d’un humain, d’un chimpanzé, d’un babouin et d’un représentant Néanderthal, étant donné le caractère plastique des tissus cortical et trabéculaire et les dynamiques de modelage et remodelage osseux au cours de la vie pour s’adapter à l’environnement local des charges, le développement d’une étude holistique de l’endostructure de la patella, ponctuellement accompagnée d’une approche de sous échantillonnage lorsque nécessaire, pourrait permettre de révéler des informations fonctionnelles pour la reconstruction de l’environnement des charges du genou chez les taxons fossiles. De telles informations peuvent enrichir la discussion sur les forces évolutives ayant configuré l’articulation du genou en relation avec les modes posturaux et locomoteurs. Elle pourrait également contribuer à l’identification taxinomique de spécimens fossiles isolés.This contribution is a short review of the functional significance of the patella in extant catarrhines and extinct hominins and of current functional, adaptive and evolutionary-related questions concerning the fossil hominin record. The patella plays a key functional role in the knee joint and thus reflects habitual postural and locomotion modes. However, patellar remains are rare in the hominin fossil record and it is still unclear whether and how their differences in shape and proportions compared to extant humans affect knee kinesiology. Here, we illustrate with a first example from a sample of human, Pan, Papio and Neanderthal patellae that the development of a "whole-bone" endostructural analysis has the potential to provide relevant functional information for reconstructing the knee loading environment in fossil taxa, combined, whenever necessary, with a subsampling approach. This method relies on the plastic nature of the cortical and trabecular bony tissues and the modelling and remodelling dynamics during life to adjust structurally to the site-specific loading environment. This kind of information would bring new contributions not only to ongoing discussions on the evolutionary forces that shaped the knee joint in association with postural and locomotor adaptations, but also to the tentative taxonomic identification of isolated fossil specimens

Caractéristiques endostructurales du squelette postcrânien de Paranthropus robustus. Implications taxinomiques, fonctionnelles et paléobiologiques

La présence d'éléments postcrâniens fragmentaires et/ou isolés non associés de façon tangible avec des restes crânio-dentaires rend souvent incertaine la discrimination entre Paranthropus et Homo. Ceci est vrai pour plusieurs assemblages fossilifères sud-africains, où la paléobiodiversité hominine s'est révélée plus importante qu’estimée auparavant. L'attribution taxinomique des restes postcrâniens repose généralement sur la morphologie externe, alors que l'agencement interne des tissus cortical et trabéculaire reflète une composante évolutive-adaptative sous contrôle génétique (bauplan), ainsi qu’une composante biomécanique à caractère fonctionnel. Au moyen de techniques d'imagerie noninvasive à haute résolution et d'analyses 3D, en collaboration avec la South African Nuclear Energy Corporation (Necsa) de Pelindaba, nous avons entrepris un projet visant l'extraction virtuelle et la quantification de caractéristiques d’intérêt taxinomique, fonctionnel et paléobiologique de l'endostructure osseuse d'éléments postcrâniens isolés communément attribués à P. robustus. Ce projet prend aussi en compte les variations observées chez d'autres hominidés actuels (notamment, Homo et Pan) et fossiles (Homo et Australopithecus). Les éléments considérés à ce jour incluent l'humérus distal (TM 1517g, SK 24600, SKX 10924), l'ulna proximale (TM 1517e), l'ilium (TM 1605, SK 50), le fémur proximal (SK 82, SK 97, SK 3121, SKW 19) et la patella (SKX 1084). Les résultats préliminaires de l'humérus distal et de la patella offrent un exemple de signal contrasté entre morphologie externe et interne (paramètres de géométrie de section, distribution topographique de l'os cortical, propriétés du réseau trabéculaire), ce qui montre l'intérêt de cette approche. En plus des proportions entre l’épaisseur corticale supérieure et inférieure, notre analyse du col fémoral prend en compte pour la première fois l'organisation des aspects antérieur et postérieur examinés le long de la portion entre le grand trochanter et la tête fémorale, ce qui a permis de mettre en évidence des caractéristiques proches de celles du fémur humain mais aussi propres à P.r

Functional implications of the differences in the inner structural organization between the Neanderthal and the modern human patella

The Neanderthal patellar morphology differs from that of recent humans by being anteroposteriorly thicker and by showing more symmetric articular facets and higher angles. However, it is still unclear to what extent these differences affect knee kinesiology. By using micro-focus X-ray tomography, we qualitatively and quantitatively characterized the inner conformation of six adult Neanderthal patellae from the OIS 5e site of Krapina, Croatia, and compared their pattern to the configuration di..

The Neandertal (Krapina and Regourdou 1), fossil modern human (Chancelade 1) and extant human patella: an insight from inside

Evolutionary endostructural patterns of the cortical and cancellous tissues of the postcranial skeleton are commonly investigated for inferring functional behaviours in extinct hominin taxa and past human populations. Information on the endostructural arrangement of the patellar bone has the potential of revealing individual- and/or taxon-specific aspects of the knee biomechanics. However, evidence on its inner conformation extracted from human fossil specimens is nearly non-existent. The present pilot study aims at characterising the endostructural pattern of two Neandertal (from Krapina, Croatia, and Regourdou, France) and one anatomically modern fossil human (from Chancelade, France) adult patellae and to compare their signal with the recent human condition. In the context of the gracilisation trend of the human skeleton occurred from the late Pleistocene, we expect (i) the two Neandertal patellae showing a higher amount of cortical bone compared to the fossil modern and the recent human conditions, (ii) the fossil modern patella showing a higher amount of cortical bone compared to the comparative sample, (iii) the cancellous network being relatively homogeneous between the two Neandertal individuals but distinguishable from that of the fossil modern human representative and of the comparative sample, and that (iv) the structural organisation revealed by the fossil modern patella is distinguishable from the recent human condition. For assessing the endostructural organisation of the selected patellae, we used non-invasive techniques of high resolution virtual imaging. The results do not support the first hypothesis, as marked differences have been found between the two Neandertal specimens. The second hypothesis is supported for the anterior surface, but not for the posterior surface. The third hypothesis is supported for the superior and the lateral regions of the patellar bone but for the inferior and medial portions. Finally, the fourth hypothesis is supported, but the cancellous organisation of the two Neandertal representatives is closer to the extant human pattern than to the Magdalenian specimen. Despite the generalised lack of comparable information from the human fossil record, we consider the present results of potential interest for future research of paleobiomechanical, paleobiological, and perhaps taxonomic interest, on the evolutionary structure of the human knee joint.Les patrons d’évolution de l’endostructure des tissus cortical et trabéculaire du squelette postcrânien sont communément analysés pour reconstruire les activités fonctionnelles des homininés fossiles et des populations humaines anciennes. Les informations sur l’arrangement endostructural de la patella ont le potentiel de déceler des aspects de la biomécanique du genou spécifiques à l’individu ou caractéristiques d’une espèce. Cependant, les témoins de la conformation interne extraits de spécimens humains fossiles sont quasi-inexistants. Cette étude pilote a pour objectif de caractériser le patron de l’endostructure de deux patellae néandertaliennes (de Krapina, Croatie, et Regourdou, France) et d’une patella d’un humain moderne fossile (Chancelade, France) et de le comparer à la condition humaine récente. Dans le contexte d’un processus de gracilisation du squelette humain de la fin du Pléistocène, nous formulons les hypothèses suivantes: (i) les deux patellae néandertaliennes présentent un cortex plus épais par rapport aux conditions moderne fossile et récente, (ii) la patella moderne fossile présente un cortex plus épais que mesuré dans l’échantillon comparatif, (iii) le réseau trabéculaire est relativement homogène entre les Néandertaliens mais distinct de celui du fossile moderne et de l’échantillon comparatif et (iv) l‘organisation structurale de la patella moderne fossile est distincte de la condition humaine récente. Pour analyser l’endostructure des patellae sélectionnées nous avons utilisé des techniques non-invasives d’imagerie virtuelle à haute résolution. Les résultats ne soutiennent pas la première hypothèse car des différences importantes ont été montrées entre les deux spécimens néandertaliens. La seconde hypothèse est vérifiée pour la surface antérieure mais pas pour celle postérieure. La troisième hypothèse est vérifiée pour les régions supérieure et latérale de la patella mais pas pour celles inférieure et médiale. Finalement, la quatrième hypothèse est vérifiée mais l’organisation trabéculaire des deux Néandertaliens est plus proche de la condition humaine récente que celle du spécimen magdalénien. Malgré le manque généralisé d’informations comparatives issues du registre humain fossile, nous estimons que les résultats de cette étude pilote ont un intérêt potentiel pour des recherches futures d’intérêt paléobiomécanique, paléobiologique et, peut-être, taxinomique sur l’évolution de la structure de l’articulation du genou humain

The SKX 1084 hominin patella from Swartkrans Member 2, South Africa: An integrated analysis of its outer morphology and inner structure

SKX 1084 is an isolated partial patella from Swartkrans Member 2, South Africa, attributed to a small-bodied Paranthropus robustus. This study provides complementary information on its outer conformation and, for the first time for a fossil hominin patella, documents its inner structure in the perspective of adding biomechanically-related evidence to clarify its identity. We used X-ray micro-tomography to investigate SKX 1084 and to extract homologous information from a sample of 12 recent human, one Neanderthal, and two adult Pan, patellae. We used geometric morphometrics to compare the outer equatorial contours. In SKX 1084, we identified two cancellous bony spots suitable for textural assessment (trabecular bone volume fraction, trabecular thickness, degree of anisotropy), and two related virtual slices for measuring the maximum cortico-trabecular thickness (CTT) of the articular surface. SKX 1084 shows a more complex articular shape than that for Pan, but still simpler than typical in Homo sapiens. At all sites, its CTT is thinner compared to Pan and approaches the condition in humans. This is also true for the expanded volume of the cancellous network. However, at both investigated spots, SKX 1084 is systematically intermediate between Homo and Pan for trabecular bone volume fraction and trabecular thickness, a pattern already shown in previous analyses on other Paranthropus postcranial remains. In the absence of any structural signal from patellae unambiguously sampling Paranthropus, as well as of comparable evidence extracted from specimens representing early Homo, our results do not allow rejection of the original taxonomic attribution of SKX 1084

Identification of functionally-related adaptations in the trabecular network of the proximal femur and tibia of a bipedally-trained Japanese macaque

The axial and appendicular skeleton of Japanese macaques (Macacca fuscata) trained to adopt ipedal posture and locomotion display a number of functionally-related external and internal macro- and micro-morphological changes, including site-specific cortical and trabecular bone adaptations. In this study we use high-resolution microtomography scanning to analyse the 3D distribution of trabecular architecture of the proximal femur and proximal tibia of Sansuke, a male individual trained in bipedal performances for eight years, as well as five wild individuals. The distribution and architecture of trabecular bone in the femoral head of Sansuke is distinct from that found in wild M. fuscata individuals, with a unique bone reinforcement around the region of the fovea capitis. Conversely, wild individuals exhibit two pillar-like, high-density structures (converging in an inverted cone) that reach distinct regions of the posterior and anterior surfaces of the femoral head. For Sansuke’s proximal tibia, contrary to previous observations from the cortico-trabecular complex distribution at the plateau, our results do not show a more asymmetric distribution between medial and lateral condyles with a medial reinforcement. Additionally, relative bone volume in this region is not significantly higher in Sansuke. However, we observed a slightly more medially placed bone reinforcement in the lateral condyle compared to the wild individuals as well as a slightly higher trabecular bone anisotropy in the medial than in the lateral condyle not observed in the wild individuals. These analyses provide new evidence about the nature and extent of functionally-related adaptive arrangements of the trabecular network at the coxofemoral and the knee joints in individuals recurrently experiencing atypical load

The TM 1517 odontoskeletal assemblage from Kromdraai B, South Africa, and the maturational pattern of Paranthropus robustus

The holotype of Paranthropus robustus was discovered by R. Broom in 1938 in an outcrop of bone breccia at the cave site of Kromdraai B, in Gauteng, South Africa [1]. It consists of the left half of a cranium (TM 1517a) and an associated right mandibular corpus (TM 1517b), both bearing teeth, and of seven isolated teeth (a LLP3, a LLP4 and the series URP3-M3 labelled as TM 1517c). A few weeks later, close to the block containing the cranial remains, Broom identified four postcranial elements: the distal end of a right humerus (TM 1517g), the partial proximal end of a right ulna (TM 1517e), and two toe bones (TM 1517k and TM 1517o), all at the time attributed to the same young individual represented by the cranial remains. However, the distal foot phalanx TM 1517o was subsequently attributed to a baboon. While the holotype has been variously referred to as a 'young female', a 'young adult', as 'probably male and immature', or as a 'late adolescent', it certainly represents a dentally immature individual. Since these early descriptions, no study has explored the possibility that the associated postcranial remains preserve evidence of active bone growth or recent epiphyseal closure. Clearly, however, such information would either strengthen, or challenge the idea that the craniodental and postcranial remains belong to a single P. robustus individual and, importantly, might provide the first evidence about the odontoskeletal maturational pattern of this fossil taxon. Accordingly, we performed a micro-XCT-based study aimed at characterising the inner structure of the distal humerus TM 1517g, the proximal ulna TM 1517e and the distal hallucial phalanx TM 1517k. Our 2-3D analyses show that the distal humerus was likely completely fused, while the proximal ulna still displays a faint remnant of fusion, and the distal hallucial phalanx shows evidence of still growing bone. These findings, as well as the observation that the distal humerus and the proximal ulna fit anatomically and morpho-dimensionally [2], provide support for the original attribution of the cranial and the three postcranial remains from Kromdraai B to a single individual representing the P. robustus type specimen. Using extant human dental standards, the age at death estimate of TM 1517 is of 16.5±3 years if based on the LM2 (not fully closed distal apices) and LM3 root developmental stages (root formation stage between half and three-quarters completed). The skeletal age ranges between 14 and 18 years, for a male, and between 11 and 15 years, for a female individual. When a chimpanzee dental growth pattern is considered, TM 1517 fits the c. 10.5 years 'older juvenile' group [3], while chimpanzee skeletal maturity standards place it between 7.95 and 13.5 years. Interestingly, in humans fusion of the distal hallucial phalanx commonly slightly precedes that of the distal humerus. However, a sequence of distal humerus-distal hallucial phalanx-proximal ulna fusion, as displayed by TM 1517, is usually observed in Pan. Taken together, this new evidence for TM 1517 more closely resembles the chimpanzee condition for maturational patterning. This finding is broadly in line with the evidence observed for Australopithecus sediba [4] and Homo erectus from Nariokotome [5]. Nevertheless, since P. robustus seems characterised by sexual bimaturism (with the males experiencing prolonged growth), the uncertain sex attribution of TM 1517 still represents a limiting interpretative factor

Inner structural organization of the distal humerus in Paranthropus and Homo

The taxonomic attribution of isolated hominin distal humeri has been a matter of uncertainty and disagreement notwithstanding their relative abundance in the fossil record. Four taxonomically-based morphotypes, respectively representing P. boisei, P. robustus, non-erectus early Homo and H. erectus, have been identified based on the cross-sectional outer shape variation of an assemblage of Plio-Pleistocene eastern and southern African specimens (Lague, 2015). However, the existence of possible differences between Paranthropus and Homo in the inner structural organisation at this skeletal site remains unexplored. We used noninvasive imaging techniques to tentatively characterize the endostructural organization of five early Pleistocene distal humeri from South Africa (TM 1517g, SK 24600, SKX 10924, SKX 34805) and Ethiopia (Gombore IB), which have been variably attributed to Paranthropus or Homo. While the investigated specimens reveal diverse degrees of inner preservation related to their taphonomic and diagenetic history, in all but SK 24600 from Swartkrans we could comparatively assess some geometric properties at the most distal cross-sectional level (%CA, Ix/Iy, Imax/Imin) and quantify cortical bone thickness topographic variation across the preserved shaft portions by means of a 2-3D Relative Cortical Thickness index. Whenever possible, we also provided details about the site-specific organization of the cancellous network and measured the same parameters in a comparative sample of twelve adult extant humans. For most features, our results indicate two main patterns: the first includes the specimens TM 1517g, SKX 10924 and SKX 34805, while the second endostructural morphotype sets apart the robust Homo aff. erectus Gombore IB specimen from Melka Kunture, which more closely resembles the condition displayed by our comparative human sample. Notably, marked differences in the amount and pattern of proximodistal cortical bone distribution have been detected between Gombore IB and SKX 34805 from Swartkrans. Given its discordant outer and inner signatures, we conclude that the taxonomic status of SKX 34805 deserves further investigations

Cortical bone distribution of the proximal phalanges in great apes: implications for reconstructing manual behaviours

Primate fingers are typically in direct contact with the environment during both locomotion and manipulation, and aspects of external phalangeal morphology are known to reflect differences in hand use. Since bone is a living tissue that can adapt in response to loading through life, the internal bone architecture of the manual phalanges should also reflect differences in manual behaviours. Here, we use the R package Morphomap to analyse high‐resolution microCT scans of hominid proximal phalanges of digits 2–5 to determine whether cortical bone structure reflects variation in manual behaviours between bipedal (Homo), knuckle‐walking (Gorilla, Pan) and suspensory (Pongo) taxa. We test the hypothesis that relative cortical bone distribution patterns and cross‐sectional geometric properties will differ both among extant great apes and across the four digits due to locomotor and postural differences. Results indicate that cortical bone structure reflects the varied hand postures employed by each taxon. The phalangeal cortices of Pongo are significantly thinner and have weaker cross‐sectional properties relative to the African apes, yet thick cortical bone under their flexor sheath ridges corresponds with predicted loading during flexed finger grips. Knuckle‐walking African apes have even thicker cortical bone under the flexor sheath ridges, as well as in the region proximal to the trochlea, but Pan also has thicker diaphyseal cortices than Gorilla. Humans display a distinct pattern of distodorsal thickening, as well as relatively thin cortices, which may reflect the lack of phalangeal curvature combined with frequent use of flexed fingered hand grips during manipulation. Within each taxon, digits 2–5 have a similar cortical distribution in Pongo, Gorilla and, unexpectedly, Homo, which suggest similar loading of all fingers during habitual locomotion or hand use. In Pan, however, cortical thickness differs between the fingers, potentially reflecting differential loading during knuckle‐walking. Inter‐ and intra‐generic variation in phalangeal cortical bone structure reflects differences in manual behaviours, offering a comparative framework for reconstructing hand use in fossil hominins