Evolutionary anatomy of the Neandertal ulna and radius in the light of the new El Sidrón sample

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Abstract

This paper aims to improve our understanding of the phylogenetic trait polarity related to hominin forearm evolution, in particular those traits traditionally defined as “Neandertal features.” To this aim, twelve adult and adolescent fragmented forelimb elements (including ulnae and radii) of Homo neanderthalensis recovered from the site of El Sidrón (Asturias, Spain) were examined comparatively using three-dimensional geometric and traditional morphometrics. Mean centroid size and shape comparisons, principal components analysis, and phylogenetic signal analysis were undertaken. Our investigations revealed that the proximal region of the ulna discriminated best between Neandertals and modern humans, with fewer taxonomically-informative features in the distal ulna and radius. Compared to modern humans, the divergent features in the Neandertal ulna are an increase in olecranon breadth (a derived trait), lower coronoid length (primitive), and anterior orientation of the trochlear notch (primitive). In the Neandertal radius, we observe a larger neck length (primitive), medial orientation of the radial tubercle (secondarily primitive), and a curved diaphysis (secondarily primitive). Anatomically, we identified three units of evolutionary change: 1) the olecranon and its fossa, 2) the coronoid–radius neck complex, and 3) the tubercle and radial diaphysis. Based on our data, forearm evolution followed a mosaic pattern in which some features were inherited from a pre-Homo ancestor, others originated in some post-ergaster and pre-antecessor populations, and other characters emerged in the specific Homo sapiens and H. neanderthalensis lineages, sometimes appearing as secondarily primitive. Future investigations might consider the diverse phylogenetic origin of apomorphies while at the same time seeking to elucidate their functional meaning.

Introduction

It often has been assumed that many of the postcranial features that distinguish anatomically modern humans (AMH) and Neandertals correspond to specializations in Neandertals (Aiello and Dean, 1990, Vandermeersch and Trinkaus, 1995, Weaver, 2009, De Groote, 2011), with little consideration of phylogenetic polarity. The Neandertal body has been characterized as muscularly robust, with a wide trunk and shortened distal limb segments as an adaptation to cold climates (Howell, 1952, Coon, 1962, Le Gros Clark, 1964, Badoux, 1965, Trinkaus, 1981, Ruff, 1991, Holliday, 1997, Churchill, 1998, Pearson, 2000, Steegmann et al., 2002, Weaver, 2003, Weaver, 2009), although further detailed analyses do not support the thermoregulatory hypothesis (Franciscus, 2003, Holton and Franciscus, 2008, Rae et al., 2011). Alternatively, high activity levels in diverse ecological environments (Sorensen and Leonard, 2001, Churchill, 2006) or simply random processes (e.g., genetic drift; Weaver et al., 2007) have been proposed as reasons for Neandertal phenotypic idiosyncrasy (Rosas et al., 2006).

The scarcity of postcranial remains predating classic early Upper Pleistocene human fossils has hindered tracing of the precedents of so-called “Neandertal features,” making it difficult to establish a proper sequence of phylogenetic polarity. A critical evaluation of some of these features proposes that many of them are, in fact, primitive characters inherited from ancestors (yet to be determined), rather than Neandertal specializations (Trinkaus, 1981, Trinkaus, 1983, Trinkaus, 2006, Carretero et al., 1999, De Groote, 2011, Rosas et al., 2015). Such interpretations have been supported through study of more complete samples, especially from the Sima de los Huesos (Sierra de Atapuerca, Spain), which has allowed the development of a clearer model for the evolution of the Neandertal lineage (Bermúdez de Castro, 1986, Arsuaga et al., 1991, Arsuaga et al., 2015, Carretero et al., 1999, Rosas et al., 1991, Rosas, 2001, Martinón-Torres et al., 2012). These studies reinforce the need to re-examine Neandertal postcranial traits and their functional significance because some of them may have originated in relatively warm environments rather than the cold conditions popularly associated with Neandertals.

What is becoming clear is that the wide body of Neandertals (Ruff, 1994, Carretero et al., 2004), together with their proportionally wide epiphyses (Pearson, 2000, De Groote, 2011) and thick cortical areas of the long bones (Arsuaga et al., 2015), all represent aspects of a plesiomorphic body form (Gómez-Olivencia et al., 2009, Arsuaga et al., 2015). When examining the Neandertal skeleton, it is still not clear which of characteristics are real autapomorphic traits, nor how they developed on the basis of this primitive architecture. Investigation of the phylogenetic origins of Neandertal postcranial morphology has become a topic of intense interest (e.g., Arsuaga et al., 2015, Rosas et al., 2015, Rosas et al., 2016), especially because a recent detailed analysis of Homo antecessor specimens revealed the presence of some “Neandertal features” in late Lower Pleistocene samples (Martinón-Torres et al., 2007, Bermúdez de Castro et al., 2012, Bermúdez de Castro et al., 2015, Gómez-Robles et al., 2015).

Forearm bones are ideal for exploring questions related to trait polarity and evolution in Neandertals. First, clear morphological differences between the ulna and the radius of Neandertals and AMH have been revealed (Trinkaus and Churchill, 1988, Vandermeersch and Trinkaus, 1995, Pearson and Grine, 1997; De Groote, 2011), showing a greater number of primitives features in Neandertals (Churchill et al., 1996, Arsuaga et al., 2015, Rodríguez et al., 2016). Second, and very importantly, the proposed thermoregulatory adaptation to cold climates could directly affect the anatomy of the forearm, basically through a shortening of its length in comparison to those of Archaic Modern Humans (Qazfeh and Skhull) and Upper Paleolithic hominins (Trinkaus, 1981, Holliday and Trinkaus, 1991, Holliday, 1997, Holliday, 1999). Thus, the forearm contains a number of characteristics that make it a good anatomical system to explore the phylogenetic origin of “Neandertal features,” whether they are primitive retentions, properly derived features, or evolutionary reversions.

When compared to AMH, the Neandertal ulna is characterized by a greater anteroposterior shaft curvature and a larger proximal epiphysis with a more anterior trochlear notch orientation (Vandermeersch and Trinkaus, 1995, Churchill et al., 1996, Yokley and Churchill, 2006, De Groote, 2011). Moreover, it has a lower anteroposterior diameter of the coronoid process, a more distal brachialis muscle position (Churchill et al., 1996, Yokley and Churchill, 2006), and a well-defined crest for attachment of the pronator quadratus muscle, while the interosseous crest is poorly developed. Finally, the shaft is relatively gracile in comparison to epiphyseal size, being more rounded at midshaft because of the small interosseous crest (Aiello and Dean, 1990).

From a phylogenetic perspective, anterior orientation of the trochlear notch and a relatively large olecranon process are considered primitive characters (Churchill et al., 1996). These features are present in all Sima de los Huesos ulnae (Arsuaga et al., 2015), in the African fossil KNM-BK 66 (Homo ergaster, Middle Pleistocene, Kenya; Solan and Day, 1992) and, interestingly, in the Klasies River Mouth fossil (African Upper Pleistocene, South Africa; Churchill et al., 1996). Furthermore, trochlear notch orientation and olecranon size are also configured similarly in Australopithecus sediba (Churchill et al., 2013), Australopithecus afarensis (Drapeau et al., 2005), and Ardipithecus ramidus (White et al., 2009). However, the ulnae of Skhul and Qafzeh (early AMH, Israel) show a derived anatomy, as is also found in 90% of AMH (Churchill et al., 1996, Groves, 1998).

Features that define Neandertal radial morphology include pronounced mediolateral shaft curvature (Vandermeersch and Trinkaus, 1995, Carretero et al., 1999, De Groote, 2011, Arsuaga et al., 2015, Rodríguez et al., 2016), together with a medial orientation of the radial tubercle (Trinkaus and Churchill, 1988, Vandermeersch and Trinkaus, 1995, De Groote, 2011, Arsuaga et al., 2015, Rodríguez et al., 2016). A more marked crest of the supinator muscle enthesis, anteroposterior expansion of the radial head, greater neck length, and a more projected styloid process also characterize the Neandertal radius (De Groote, 2011). However, the differences between AMH and Neandertals are appreciated best in whole radial morphology rather than in a feature by feature comparison, when clear overlaps between the two species are found (De Groote, 2011). Large mediolateral shaft curvature (Vandermeersch and Trinkaus, 1995, Carretero et al., 1999, De Groote, 2011) has been observed in most of the radii found in the pre-Neandertal population of the Sima de los Huesos (Arsuaga et al., 2015, Rodríguez et al., 2016), but not in specimens of H. antecessor (final Lower Pleistocene, Sierra de Atapuerca, Spain; Carretero et al., 1999) or in AMH populations. Defining the polarity of mediolateral radial shaft curvature is complicated because it is quite variable in the different species of Australopithecus: straight in Au. afarensis but curved in Au. sediba (Churchill et al., 2013), Australopithecus anamensis (Ward et al., 2001), and Ar. ramidus (White et al., 2009).

A long radial neck is found in Neandertals, Australopithecus (except the Au. sediba specimen MH2; Churchill et al., 2013), Paranthropus (Dominguez-Rodrigo et al., 2009), H. antecessor, and most of the Sima de los Huesos specimens (Carretero et al., 1999, Arsuaga et al., 2015, Rodríguez et al., 2016). Thus, a long radial neck could be considered a primitive hominin condition, while a shorter radial neck is a derived state found in AMH. Finally, the medial orientation of the radial tubercle typical of Neandertals (Trinkaus and Churchill, 1988, Vandermeersch and Trinkaus, 1995, De Groote, 2011) has been observed in the Au. afarensis (AL 288-1), Paranthropus (OH 80-11), early Homo (OH 62 and KNM-ER 1500), and 20% of the Sima de los Huesos radii (Rodríguez et al., 2016). In contrast, H. antecessor, the remaining 80% of the Sima de los Huesos radii, and the Cave of Hearts and Klasies River Mouth radii have an anteromedial orientation of the radial tubercle, as in AMH (Tobias, 1971, Pearson and Grine, 1997, Carretero et al., 1999, Rodríguez et al., 2016). The apparent reappearance of a medially oriented radial tubercle in Neandertals, mostly absent in their hypothetical direct ancestors, suggests a reversion to the primitive condition (Carretero et al., 1999, Rodríguez et al., 2016), similar to what was proposed for olecranon fossa breadth in the AMH humerus (Rosas et a., 2015) or the reorientation of the acromial clavicle in Neandertals (Rosas et al., 2016).

Here, we explore the Neandertal phenotype further, discerning between the retained primitive components and the traits that have emerged in the stepwise process of Neandertal specialization in the Pleistocene. We present and analyze the Neandertal sample of ulnae and radii from El Sidrón (Rosas et al., 2013) in a broad phylogenetic context, using traditional and geometric morphometric techniques. We have four specific aims. First, we test whether the new ulna and radius fossils from the El Sidrón (Asturias, Spain) site display the set of features previously established as being specific to Neandertals. Second, we assess intra-group morphological variability to evaluate the degree of fixation of those features within Neandertal populations. We expect low variation in the El Sidrón sample because these individuals derived from a biological unit with close familial ties (Rosas et al., 2006, Lalueza-Fox et al., 2012, Dean et al., 2013, Ríos et al., 2015). Third, we test the null hypothesis that the Neandertal forearm maintains a mostly primitive anatomy, in contrast to the largely derived anatomy of modern human populations. A further implication is that the ulna retains a mostly primitive anatomy in every hominin species other than anatomically modern humans. Consequently, it is to be expected that the three-dimensional (3D) configuration of the Neandertal ulnae groups closely with other hominin remains in morphospace. Finally, we explore whether the radius, which has a more scarce fossil record, also groups alongside other hominins.

Section snippets

Materials and methods

El Sidrón is a karstic site located in the municipality of Piloña (Asturias, Spain; Fortea et al., 2003, Rosas et al., 2006, de la Rasilla et al., 2011). The fossil assemblage comprises more than 2400 remains and has been dated to 49 ka (Wood et al., 2013). Further details of the sample and site can be found elsewhere (Rosas et al., 2012, Rosas et al., 2015). Fragments of six right and seven left ulnae (Table 1) and five right and six left radii (Table 2) from El Sidrón are described here.

Ulna 1 (SDR-054 + SDR-055 + SDR-056; Figs. 2 and 3)

This is an almost complete right ulna of a young adult that lacks only the lateral region of the ulnar head. The fusion of the distal epiphysis is not complete. Muscle entheses and the interosseous crest are not very marked.

Ulna 2 (SDR-057 + SDR-058; Figs. 3 and 4)

This is a gracile left adult ulna. The trochlear notch is incomplete and the distal portion of the diaphysis is absent. This ulna shows a large brachialis muscle enthesis, and its interosseous crest is the most marked in the sample.

Ulna 3 (SDR-059 + SDR-060 + SDR-061 + SDR-148 + SD-1051c; Figs. 3 and 4)

This is a left adult ulna that preserves

Discussion

We observed that most of the features in the Neandertal ulna had a primitive configuration, with the exception of the olecranon process. The Neandertal radius largely displayed a primitive morphology, but we suggest that some features may be homoplastic due to character reversals (i.e., they are secondarily primitive).

Conclusion

In summary, although the radius and ulna have a very close anatomical relationship, with the bones articulating proximally and distally as well as being connected via the interosseous membrane, from a phylogenetic point of view both bones show a different pattern of evolution. Some ulnar and radial characters have evolved in a mosaic fashion, giving rise to the morphologies that define the Neandertal and AMH forearms. In accordance with Churchill et al. (1996) and Arsuaga et al. (2015), our

Acknowledgments

We thank all of the excavation team working at El Sidrón, as well as the other members of the Group of Paleoanthropology MNCN-CSIC. We are grateful to the NESPOS Society and the professionals behind it for providing CT data. We are very thankful to Juan Francisco Pastor (Universidad de Valladolid) for allowing access to the modern humans collection and to A. Balzeau and A. Florent from the Musée de l'Homme for providing the CT data from La Chapelle aux Saints. Finally, we are grateful for the

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