Knee joint loading diversity in South African hominins as evidenced by the trabecular structure of the distal femur

Abstract

A valgus knee has consistently been considered as evidence for bipedalism in Australopithecus, indicating an extended knee posture. This knee characteristic has been central to debates surrounding the potential retention of climbing abilities in the locomotor repertoire of A. afarensis [1]. Distinctions can be observed in the distal femoral morphology among australopiths, such as varying degrees of anterior projection of the lateral patellar lip, as well as differences from Homo, including the anterior expansion of the patellar surface [2]. Relying solely on the external morphology of the knee epiphyses may have limitations in discerning subtle differences in knee biomechanics among hominins with diverse locomotor repertoires. Examining the variation in the trabecular bone may offer additional insights into the biomechanical differences of the fossil hominin knees. We analyse the internal morphology of StW 318 and TM 1513 distal femora, attributed to A. africanus, and the U.W. 88-63, attributed to A. sediba. A comparative sample of Homo sapiens (N=15), Gorilla gorilla (N=14), Pan troglodytes verus (N=15), and Pongo spp. (N=9) was used. All specimens were scanned via micro-CT and segmented using medical image analysis (MIA) clustering segmentation [3]. A holistic morphometric analysis (HMA) was used to quantify relative trabecular bone density (rBV/TV) in the distal femoral epiphyses [4]. To statistically compare variation between groups, a canonical holistic morphometric analysis (cHMA) was applied [5]. Variation in the trabecular structure was further compared via principal component analyses (PCA). Each fossil hominin specimen was variably preserved, and analysis was restricted as follows: StW 318 – only the lateral condyle; TM 1513 – whole epiphysis except for the missing medial epicondyle; U.W. 88-63 – region under the patellar surface. Results of the PCA separate H. sapiens by high rBV/TV posteroinferiorly in the femoral condyles, laterally under the patellar surface and higher rBV/TV in the lateral compared to the medial condyle. This distribution pattern reflects higher lateral loading due to extended knee postures. In African apes, high rBV/TV is concentrated posterosuperiorly in the femoral condyles, medially on the patellar surface, and it is higher in the medial compared to the lateral condyle. This distribution pattern reflects higher medial loading due to flexed knee postures. Pongo displays a more homogenous rBV/TV distribution, suggesting more diverse postural and locomotor behaviour. All extinct taxa display a unique set of human-like and ape-like characteristics. StW 318 exhibits a trabecular distribution under the patellar surface, in the lateral epicondyle, and in the posteroinferior volumes of the lateral condyle, falling somewhere between Pan and Pongo in the PCA and suggesting the knee was loaded in flexed postures, but possibly to a lesser extent than in African ape. The distribution beneath the insertion of gastrocnemius muscle resembles that of H. sapiens, suggesting a potentially same level of muscular involvement during bipedal walking. TM 1513 shows high rBV/TV in the distal volumes of both femoral condyles, suggesting extended knee postures. The higher rBV/TV values in the medial compared to the lateral condyle are consistent with higher medial knee compartment loading. The rBV/TV concentration beneath the insertions of the gastrocnemius muscle is again more like that of H. sapiens. U.W. 88-63 exhibits a trabecular distribution falling close to Pongo. High rBV/TV is concentrated more laterally compared to A. africanus and African apes under the patellar surface, supporting the functional interpretation of extended knee postures during bipedal locomotion with a degree of knee flexion that differs from A. africanus and African apes. These findings underscore the diversity in knee joint loading among South African hominins. For access to specimens in their collections, we thank the follow ing individuals/institutions: Max Planck Institute for Evolutionary Anthropology (C. Boesch, J-J. Hublin); Museum für Naturkunde – Leibniz Institute for Evolution and Biodiversity Science (F. Mayer, C. Funk); Powell-Cotton Museum (I. Livne); Royal Museum for Central Africa (E. Gilissen); University of Florence (J. Moggi-Cecchi, S. Bortoluzzi); Johann-Friedrich-Blumenback-Institute for Zoology and Anthropology, Georg-August University, Goettingen (B. Grosskopf); Frankfurt Senckenberg Museum (V. Volpato); University of the Witswatersand (L. Berger, B. Zipfel); Science Academy of the Czech Republic (J. Svoboda). We thank the Editor-in-Chief, J. Saers and one anonymous reviewer for these constructive comments that greatly improved our manuscript. This project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 819960).

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