The morphology and evolutionary history of the glenohumeral joint of hominoids: A review.

Received: 6 December 2017 | Revised: 11 June 2018 | Accepted: 18 June 2018 DOI: 10.1002/ece3.4392 REVIEW ARTICLE The morphology and evolutionary history of the glenohumeral joint of hominoids: A review Julia Arias-Martorell Animal Postcranial Evolution Lab, Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury, UK Correspondence Julia Arias-Martorell, Animal Postcranial Evolution Lab, Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Marlowe Building, Canterbury, Kent CT2 7NR, UK. Email: Funding information H2020 Marie Skłodowska-Curie Actions, Grant/Award Number: 703608 Abstract The glenohumeral joint, the most mobile joint in the body of hominoids, is involved in the locomotion of all extant primates apart from humans. Over the last few decades, our knowledge of how variation in its morphological characteristics relates to different locomotor behaviors within extant primates has greatly improved, including features of the proximal humerus and the glenoid cavity of the scapula, as well as the muscles that function to move the joint (the rotator cuff muscles). The glenohumeral joint is a region with a strong morphofunctional signal, and hence, its study can shed light on the locomotor behaviors of crucial ancestral nodes in the evolutionary history of hominoids (e.g., the last common ancestor between humans and chimpanzees). Hominoids, in particular, are distinct in showing round and relatively big proximal humeri with lowered tubercles and flattened and oval glenoid cavities, morphology suited to engage in a wide range of motions, which enables the use of locomotor behaviors such as suspension. The comparison with extant taxa has enabled more informed functional interpretations of morphology in extinct primates, including hominoids, from the Early Miocene through to the emergence of hominins. Here, I review our current understanding of glenohumeral joint functional morphology and its evolution throughout the Miocene and Pleistocene, as well as highlighting the areas where a deeper study of this joint is still needed. KEYWORDS evolutionary morphology, glenohumeral morphology, hominins, hominoids, locomotion, Miocene apes 1 | I NTRO D U C TI O N answering such question. Theories on the origin of bipedalism, which try to elucidate the locomotor behavior exhibited by the last com- The evolution of primate locomotion and, especially, ape locomo- mon ancestor (LCA) between humans and chimpanzees, range from tion is fundamental to the understanding of human origins. Its im- characterizing the LCA as gorilla and chimpanzee-like (thus knuckle- portance resides on a central question of the discipline: How and walking; e.g., Richmond & Strait, 2000); as largely arboreal and simi- when did we start walking on two feet? Bipedalism is a defining lar to orangutans today (e.g., Thorpe, Holder, & Crompton, 2007); or feature of being humans, and the study of the evolution of primate engaging in a more heterogeneous and generalized pool of arboreal locomotor behaviors, with an emphasis on how morphological behaviors (climbing, clambering, bridging) as seen in the living ar- variation throughout the skeleton may relate to function, is key to boreal primates (e.g., Arias-Martorell, Potau, Bello-Hellegouarch, & This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Author. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;9:703–722.  www.ecolevol.org | 703 704 | ARIAS-MARTORELL Pérez-Pérez, 2015c). It is unfortunate that fossil remains throughout morphological and functional diversity across primates and how primate and, in particular, ape evolutionary history are scarce, and they generally relate to the main locomotor modes found within the thus, we lack the evidence to fully support any one theory. order. The review will then discuss in-depth key morphofunctional Among nonhuman hominoids, the forelimb is critical to a diver- characters of the proximal humerus and the glenoid cavity focus- sity of locomotor behaviors, ranging from terrestrial knuckle-walking ing on hominoids and using other primate groups to highlight differ- to suspension to ricochetal brachiation, but is largely removed from ences in morphology related to opposing locomotor behaviors (e.g., locomotion in humans. Within the forelimb, the glenohumeral joint— suspension vs. quadrupedalism). In particular, as these traits are also the articulation between the scapula’s glenoid fossa and the proximal commonly used to infer locomotor behaviors in the past, I will ad- humerus—is the primary joint involved in arm movement and the most dress this topic in the following sections dealing with the locomotion mobile joint in the body in hominoids (including Gorilla, Pan, Pongo, and evolutionary history of Miocene hominoids and hominins. The Homo, and the hylobatid family). As such, it has been the focus of mor- final section will be, as mentioned, a reflection on areas of future phological and biomechanical studies for decades and its major exter- studies and possible directions on the analysis of the glenohumeral nal morphological features have been functionally associated with the joint. use of certain locomotor behaviors in primates (Arias-Martorell, Alba, Potau, Bello- Hellegouarch, & Pérez- Pérez, 2015b; Arias- Martorell, Tallman, Potau, Bello- Hellegouarch, & Pérez- Pérez, 2015a; Arias- Martorell et al., 2015c; Kagaya, 2007; Larson, 1993, 1995, 2007a; 2 | TH E G LE N O H U M E R A L J O I NT: OV E R A LL M O R PH O LO G Y A N D FU N C TI O N Rose, 1989). Within hominoids, the high degree of glenohumeral mobility The glenohumeral joint describes the articulation between the has been widely linked to the evolution of an upright body pos- proximal humerus and glenoid cavity of the scapula (Figure 1). ture, also known as orthogrady, which involved the displace- Important features include the rotator cuff muscles, which origi- ment of the scapula onto the back of a mediolaterally wide and nate in the scapular blade (or fossae) and attach at the greater anteroposteriorly shallow thorax (e.g., Andrews & Groves, 1976; and lesser tubercles of the proximal humerus and provide stability Gebo, 1996, 2010; Keith, 1903, 1923; Ward, 2015). The scapular and movement to the joint (Figure 1). There are four rotator cuff displacement resulted in a more mobile and less stable glenohu- muscles: the subscapularis muscle, originating in the subscapular meral joint, which may move in all directions and may combine fossa of the scapula and inserting in the lesser tubercle; the su- all possible movements, from flexion and extension to abduction praspinatus muscle, originating in the supra (...truncated)