Elsevier

Journal of Human Evolution

Volume 95, June 2016, Pages 55-67
Journal of Human Evolution

Adult Neandertal clavicles from the El Sidrón site (Asturias, Spain) in the context of Homo pectoral girdle evolution

https://doi.org/10.1016/j.jhevol.2016.03.005Get rights and content

Abstract

We undertook a three-dimensional geometric morphometric (3DGM) analysis on 12 new Neandertal clavicle specimens from the El Sidrón site (Spain), dated to 49,000 years ago. The 3DGM methods were applied in a comparative framework in order to improve our understanding of trait polarity in features related to Homo pectoral girdle evolution, using other Neandertals, Homo sapiens, Pan, ATD6-50 (Homo antecessor), and KNM-WT 15000 (Homo ergaster/erectus) in the reference collection. Twenty-nine homologous landmarks were measured for each clavicle. Variation and morphological similarities were assessed through principal component analysis, conducted separately for the complete clavicle and the diaphysis. On average, Neandertal clavicles had significantly larger muscular entheses, double dorsal curvature, clavicle torsion, and cranial orientation of the acromial end than non-Neandertal clavicles; the El Sidrón clavicles fit this pattern. Variation within the samples was large, with extensive overlap between Homo species; only chimpanzee specimens clearly differed from the other specimens in morphometric terms. Taken together, our morphometric analyses are consistent with the following phylogenetic sequence. The primitive condition of the clavicle is manifest in the cranial orientation of both the acromial and sternal ends. The derived condition expressed in the H. sapiens + Neandertal clade is defined by caudal rotation of both the sternal and acromial ends, but with variation in the number of acromia remaining in a certain cranial orientation. Finally, the autapomorphic Neandertal condition is defined by secondarily acquired primitive cranial re-orientation of the acromial end, which varies from individual to individual. These results suggest that the pace of phylogenetic change in the pectoral girdle does not seem to follow that of other postcranial skeletal features.

Introduction

Clarifying whether the features frequently observed in Neandertal populations originated in the last common ancestor of Neandertals and Homo sapiens or only in the lineage leading to Neandertals (since divergence) may provide insight into morphofunctional evolution in Pleistocene hominins. Many derived features in the postcranial skeleton may be morphological consequences of body-form divergences; pelvis breadth, thorax shape, and the pectoral girdle seem to be involved in these divergences in one way or another. The Neandertal torso is large and deep (Bastir et al., 2015), traditionally perceived as a body form specialized for cold weather (Vandermeersch and Trinkaus, 1995, Churchill, 1996). The upper thorax of modern humans differs in shape from that of Neandertals, which shows more anteriorly projecting upper ribs during inspiration (Bastir et al., 2015). This in turn implies a reconfigured spatial arrangement of the pectoral girdle. In this context, study of the configuration of the clavicle through three-dimensional geometric morphometric (3DGM) analysis may help characterize variations in form and elucidate its potential covariation with other elements of the pectoral girdle.

Clavicle length is one of the characteristics that originally enabled researchers to distinguish Neandertal anatomy from that of anatomically modern humans (Boule, 1911-13, Churchill, 1994, Holliday, 1997, Larson, 2013; see Trinkaus et al., 2014 for a complete review). Supposedly, a long clavicle allows for a broad thorax. As a consequence of an enlarged chest, Vandermeersch and Trinkaus (1995) and Churchill (1996) suggested that Neandertal scapulae were positioned more laterally, with a horizontal scapular spine and a distinctive axillary-border morphology, along with more anteriorly directed tall and narrow glenoid fossae (Churchill and Trinkaus, 1990). Later, Larson (2007) suggested that the relatively long clavicles of Neandertals were also products of large chest size, as they were needed to bridge the longer distance from the sternum to the acromion. A distinctive scapulo-humeral joint shape has also been reported (Carretero et al., 1997, Lari et al., 2015). Nonetheless, Trinkaus et al. (2014) recently downplayed this evidence on the basis that relative clavicle length, appropriately scaled to body mass, maintains a constant relationship across species of the genus Homo (sensu stricto), and thus paleobiological inferences based on the study of clavicle length should be avoided.

In contrast, other experts have determined that in addition to the size of the clavicle, its shape discriminates among groups of Homo. Independent of length, clavicle morphology potentially yields insight into Homo paleobiology and evolution. For instance, Voisin (2004) stated that the Neandertal clavicle reflects the special architecture of the Neandertal shoulder, which is characterized by a high scapula in relation to the thorax. In a broader context, clavicular curvature on the dorsal view is related to shoulder position (Voisin, 2001, Voisin, 2004, Voisin, 2006a, Voisin, 2006b, Voisin, 2008, Voisin, 2010). The vast majority of hominin species (except H. sapiens) normally exhibit clavicles with two curvatures on the dorsal view: one inferior, at the lateral extremity, and one superior, at the medial extremity. The morphology of these type-II clavicles is related to a scapula that is positioned high relative to the rib cage. By contrast, most modern humans harbor clavicles with a single curvature (type I) due to the low position of the scapula in relation to the thorax (Voisin, 2001, Voisin, 2004, Voisin, 2008, Voisin, 2010); 75% of Neandertal clavicles are type II, but this morphology appears in only 15% of modern human clavicles (Voisin, 2001).

The collarbone also displays a morphological characteristic that is rarely mentioned in the literature: clavicular twist (Ashton and Oxnard, 1964, Oxnard, 1984, Aiello and Dean, 1990). This twist is defined by the line of the anterior border and is related to the orientation of the acromial end (Oxnard, 1984). Generally, modern humans exhibit low torsion, while non-human hominoids and other primates present a cranially oriented acromial end (Oxnard, 1984, Aiello and Dean, 1990). Such torsion is also evident in the hominin fossil record (Oxnard, 1984, Carretero et al., 1999, Churchill et al., 2013), together with a diaphysis twist that is marked in some Neandertals (Vandermeersch and Trinkaus, 1995, Carretero et al., 1997).

The shape of the midshaft cross section is also relevant to the morphological evolution of the human clavicle. Hominin species preceding H. sapiens exhibit an elliptical midshaft cross section with a low midshaft index (<80; [minimum diameter/maximum diameter] × 100); these clavicles have been designated as platicleidic (Carretero et al., 1997, Carretero et al., 1999). In contrast, in modern humans, the cross section at midshaft is circular, with mesocleidic morphology and a midshaft index of 80–120 (McCown and Keith, 1939, Trinkaus, 1983, Carretero et al., 1997, Carretero et al., 1999). It has been reported that 88% of Homo neanderthalensis clavicle fossils present a flattened diaphysis. In most cases, this flattening is dorsoventral (Vandermeersch and Trinkaus, 1995, Carretero et al., 1997, Carretero et al., 1999), but some craniocaudal examples have been described that are consistent with the elliptical cross section reported for Neandertals (Trinkaus, 1983, Vandermeersch and Trinkaus, 1995, Carretero et al., 1997, Carretero et al., 1999, Mersey et al., 2013).

Despite large variations in clavicle dimensions, the anatomy of isolated clavicles seems to indicate systematic differences among Homo species. However, the phylogenetic pattern of this variation remains largely unexplored. Three-dimensional geometric morphometric analysis of the clavicle as part of the pectoral girdle may shed new light onto this problem. Discovery of new, well-preserved clavicle remains from the ∼49 ka (thousands of years old) El Sidrón site (Northern Spain) (Rosas et al., 2006, Rosas et al., 2012) encouraged us to use a comparative framework to explore several questions. Do the new El Sidrón clavicle remains fit the characteristic form of Neandertal clavicles? Are there significant differences in clavicle size and shape between Neandertals and modern humans? If so, which features provide information about classification and what is the phylogenetic trait polarity of these features? Although we recognize the difficulty in establishing functional relationships through the study of isolated anatomical elements, we sought to evaluate these features in the context of the evolution of the Homo pectoral girdle. Thus, this investigation evaluated the new Neandertal clavicles from the El Sidrón site in comparison with samples of Neandertal, modern human, and chimpanzee clavicles and ATD6-50 (Homo antecessor) and KNM-WT 15000 (Homo ergaster/erectus) specimens. Using 3DGM methods complemented with classic measurements, we sought to determine the main form differences among clavicles from human species in order to improve our understanding of trait polarity in features related to Homo pectoral girdle evolution. Identification of so-called “Neandertal features” in European Lower Pleistocene populations, particularly those attributed to H. antecessor from TD6 (Atapuerca), has renewed interest in trait polarity (Martinón-Torres et al., 2007, Bermúdez de Castro et al., 2015, Gómez-Robles et al., 2015). Determining which of these features are uniquely derived (autapomorphies) and which are inherited from previous ancestors (Bermúdez de Castro et al., 2012, Bermúdez de Castro et al., 2015, Rosas et al., 2015) is a key issue in the resolution of the Homo evolutionary model.

Section snippets

The El Sidrón site

El Sidrón is a karst system located in Asturias, Spain (Fortea et al., 2003, Rosas et al., 2006, de la Rasilla et al., 2011). Since 2000, samples ∼49 ka have been recovered from this site (Wood et al., 2013), constituting the most complete Neandertal sample from the Iberian Peninsula (Rosas et al., 2006, Rosas et al., 2012). The remains were in a secondary position; the original deposit, worn out by erosion, is thought to have been either on the surface or in an upper karst level (Fortea

Brief description of the El Sidrón clavicles

Photographs of the adult El Sidrón clavicle specimens included in this study can be found in Figure 2, Figure 3, Figure 4, Figure 5, with a brief description in Table 1; SD 695g is a very small fragment of the sternal end, and is not described further below.

Discussion and conclusions

This study places new fossil clavicles recovered from El Sidrón into a comparative framework using 3DGM methods. We reassessed the form and variation of the Homo clavicle via new samples and new methods that have rarely been used to study this bone. We also revisited the phylogenetic polarity of previously considered Neandertal features due to renewed interest in these features in samples from the Lower Pleistocene (e.g., Atapuerca TD6 H. antecessor; Bermúdez de Castro et al., 2015).

We found

Acknowledgments

We are grateful to everyone who participated in the El Sidrón fieldwork seasons and to other members of the Group of Paleoanthropology MNCN-CSIC. We are grateful to the NESPOS Society and to Daniel García for providing virtual data from some of the specimens included in our analyses. Finally we are very thankful to Davorka Radovčić for giving us the facilities to study the formidable collection of Krapina. This work was funded by the Ministerio de Economía y Competitividad of Spain (

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