Journal of Human Evolution 80 (2015) 64e73
Contents lists available at ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
n site (Asturias, Spain) for The relevance of the first ribs of the El Sidro the understanding of the Neandertal thorax Markus Bastir a, *, Daniel García-Martínez a, Almudena Estalrrich a, Antonio García-Tabernero a, Rosa Huguet a, b, c, d, Luis Ríos a, e, Alon Barash f, Wolfgang Recheis g, Marco de la Rasilla h, Antonio Rosas a a
Paleoanthropology Group, Museo Nacional de Ciencias Naturales (CSIC), J. G. Abascal 2, 28006, Madrid, Spain de Paleoecologia Humana i Evolucio Social (IPHES), C/ Marcel.lí Domingo s/n e Campus Sescelades URV (Edifici W3), 43007 Tarragona, Institut Catala Spain c ria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain Area de Prehisto d Unidad asociada al CSIC, Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, Calle Jos e Gutierrez Abascal, 2. 28006 Madrid, Spain e Sociedad de Ciencias Aranzadi-Aranzadi Zientzia Elkartea, Alto de Zorroaga Bidea, 11, 20014, Donostia, Gipuzkoa, Spain f Faculty of Medicine in the Galilee, Bar Ilan University, Henrietta Szold, 8, P.O.B 1589, 1311502, Zefat, Israel g Department of Radiology, Medical University Innsbruck, Anichstrasse 35, 6020 Innsbruck, Austria h n, C/ Teniente Alfonso Martínez s/n, 33011, Oviedo, Spain Department of History, University of Oviedo, Campus del Mila b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 March 2014 Accepted 17 October 2014 Available online 3 January 2015
Reconstructing the morphology of the Neanderthal rib cage not only provides information about the general evolution of human body shape but also aids understanding of functional anatomy and energetics. Despite this paleobiological importance there is still debate about the nature and extent of var n Neandertals can be used to iations in the size and shape of the Neandertal thorax. The El Sidro contribute to this debate, providing new costal remains ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs are particularly well preserved and offer the opportunity to analyze thorax morphology in Neandertals. The aims of this paper are to present this new material, to compare the ontogenetic trajectories of the first ribs between Neandertals and modern humans, and, using geometric morphometrics, to test the hypothesis of morphological integration between the first rib n adult Neandertals are smaller in centroid and overall thorax morphology. The first ribs of the El Sidro size and tend to be less curved when compared with those of modern humans, but are similar to Kebara 2. Our results further show that the straightening of the first ribs is significantly correlated with a straightening of the ribs of the upper thorax (R ¼ 0.66; p < 0.0001) in modern humans, suggesting modularity in the upper and lower thorax units as reported in other hominins. It also supports the hypothesis that the upper thorax of Neandertals differs in shape from modern humans with more anteriorly projecting upper ribs during inspiration. These differences could have biomechanical consequences and account for stronger muscle attachments in Neandertals. Different upper thorax shape would also imply a different spatial arrangement of the shoulder girdle and articulation with the humerus (torsion) and its connection to the upper thorax. Future research should address these inferences in the context of Neandertal overall body morphology. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Costal skeleton Body shape Integration Semilandmarks Homo neanderthalensis
Introduction Hypotheses about the paleobiological significance of Neandertal thorax morphology have referred to different factors ranging from
* Corresponding author. E-mail address: [email protected] (M. Bastir). http://dx.doi.org/10.1016/j.jhevol.2014.10.008 0047-2484/© 2014 Elsevier Ltd. All rights reserved.
cold adaptations, energetics and activity levels, and increased body mass (Franciscus and Churchill, 2002; Churchill, 2006) to questions related to the evolution of overall body shape (Jellema et al., 1993; mez-Olivencia et al., 2009; García-Martínez Ruff, 2002, 2010; Go et al., 2012; Bastir et al., 2013a,b). Despite its importance, the extent of differences in the size and shape of the Neandertal thorax is still not entirely clear (Franciscus and Churchill, 2002; Churchill, mez-Olivencia et al., 2009). The question of size and shape 2006; Go
M. Bastir et al. / Journal of Human Evolution 80 (2015) 64e73
differences is also important in the light of recent evidence that supports a division of the thorax into an upper and a lower part for functional, developmental and evolutionary reasons in different hominin species (Arensburg, 1991; Schmid et al., 2013; Bastir et al., 2013b, in press). While the upper part (ribs 1e5) has been related to thoracic breathing and to upper limb locomotion, the lower part (ribs 6e12) reflects features related to diaphragmatic breathing, posture and body shape as well as sub-thoracic organ content (Bastir et al., 2013b). In a pioneering quantitative analysis of isolated ribs of the Shanidar 3 Neandertal, Franciscus and Churchill (2002) suggested that the lower Neandertal thorax is larger in volume with more rounded cross sections of the lower ribs than in modern humans. Other researchers have suggested that the ribs of the lower thorax mez-Olivencia et al., 2009; in Kebara 2 are relatively large (Go García Martínez et al., 2014a). This evidence, together with a complete reconstruction of a Neandertal skeleton (Sawyer and Maley, 2005) suggests a wider lower thorax in Neandertals than in modern humans. The morphology of the upper thorax in Neandertals is considerably less well known. Sizes of the upper ribs of Kebara 2 seem to be all within or at the lower end of the range of modern humans mez-Olivencia et al., 2009; García Martínez et al., 2014a). (Go However, there is also evidence suggesting that the shape might be different. Karl Gorjanovi c-Kramberger (1906) described the first ribs of the Krapina Neandertals as particularly straight, much less curved than those of modern humans. Straightness of the first ribs in other Neandertals has also been observed in subsequent work mez(McCown and Keith, 1939; Franciscus and Churchill, 2002; Go Olivencia et al., 2009). Based on his observations of the first ribs, Gorjanovi c-Kramberger (1906) further speculated that the entire rib cage of the Krapina Neandertals probably projected more anteriorly than in modern humans (“wodurch auch der Brustkorb €lbt war”; Gorjanovic-Kramberger, 1906: 212). Thus, mehr vorgewo by predicting that the morphology of the first rib is significantly correlated to the shape of the remaining thorax, Gorjanovi cKramberger (1906) proposed an important hypothesis that is relevant to the previously mentioned studies on general thorax morphology and evolution (Franciscus and Churchill, 2002; mez-Olivencia et al., 2009). Go Anatomically, Gorjanovi c-Kramberger's (1906) hypothesis is related to the fact that the upper ribs of the thorax share an intimate relation with the respiratory system and are mutually connected by the intercostal muscles and the costo-sternal cartilages to form the chest wall (De Troyer et al., 2005). These soft-tissue connections and the need for coordinated function during lung ventilation (Franciscus and Churchill, 2002; West, 2012) probably account for the integration of the superior ribs into a morphofunctional upper thoracic unit that has been reported in different hominin species (Schmid et al., 2013; Bastir et al., 2013b). These anatomical and morphological observations justify the assumption of rib covariation patterns in modern humans and Neandertals. However, the hypothesis of Gorjanovi c-Kramberger (1906) has not yet been tested. The scantiness of upper thorax elements (for example, first ribs) in the Neandertal fossil record as well as the difficulty in properly quantifying the curved morphology of the outer rib circumference have thus far hampered a thorough analysis of this important problem. n Neandertal site in Asturias, northern Spain (Fortea The El Sidro et al., 2003; Rosas et al., 2006, 2012), which to date has produced the largest sample of Neandertal fossils in the Iberian Peninsula, also provides a significant contribution to the fossil record of thoracic elements. In addition, geometric morphometrics of 3D landmarks can be used for rigorous quantification of rib curvature, which is a key factor of overall thoracic morphology and variation
65
(García-Martínez et al., 2012, 2013; Bastir et al., 2013b). When combining geometric morphometrics and partial least squares (PLS) analysis, it is also possible to quantify and visualize shape covariation of two different anatomical systems (Rohlf and Corti, 2000; Bastir et al., 2005), such as the first rib and the remaining thorax. Thus, the aim of the present study is to describe and analyze n Neandertals within the framework a set of first ribs of the El Sidro of Gorjanovic-Kramberger's (1906) hypothesis that the morphology of the first rib morphology is significantly related to the shape of the remaining skeletal thorax. Material and methods n (Asturias, Spain) has produced a The fossil site of El Sidro considerable sample of thoracic elements, ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs SD-417, SD-1225, SD-1699 þ SD-1685 (two fragments fitted together, termed SD-1699þ onwards), SD-1767, SD-2148, SD-2172, are particularly well preserved (Fig. 1; Table 1). The ribs, like n site (Rosas et al., 2006; Bastir most of the fossils from the El Sidro et al., 2010) were covered to a variable degree with calcite concretions as a result of being embedded in the sedimentary matrix (Rosas et al., 2006, 2011). Prior to analyses, these concretions were mechanically removed to facilitate the best possible observation of ndez surface details of the bones for anatomical description (Ferna n et al., 2010). Casco Once the concretions had been removed, morphological descriptions and linear measurements (Tables 2 and 3) were under n rib fossils. The comparative sample taken for the original El Sidro included linear measurements of high quality casts of earlier Homo [KNM-WT 15000 (African Homo erectus or Homo ergaster), ATD6108, Homo antecessor] and 3D reconstructions of CT scans of the first ribs of Kebara 2 (Arensburg, 1991) and of La Ferrassie VI, a Neandertal child of approximately three to five years of age (Heim, 1982; Tompkins and Trinkaus, 1987). These data, and data taken from the literature, were compared with measurements on 3D reconstructions of CT scans of a growth series of isolated first ribs of 27 modern humans ranging from newborns to adults of both sexes, including infants (0e3 years), children (
Contents lists available at ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
n site (Asturias, Spain) for The relevance of the first ribs of the El Sidro the understanding of the Neandertal thorax Markus Bastir a, *, Daniel García-Martínez a, Almudena Estalrrich a, Antonio García-Tabernero a, Rosa Huguet a, b, c, d, Luis Ríos a, e, Alon Barash f, Wolfgang Recheis g, Marco de la Rasilla h, Antonio Rosas a a
Paleoanthropology Group, Museo Nacional de Ciencias Naturales (CSIC), J. G. Abascal 2, 28006, Madrid, Spain de Paleoecologia Humana i Evolucio Social (IPHES), C/ Marcel.lí Domingo s/n e Campus Sescelades URV (Edifici W3), 43007 Tarragona, Institut Catala Spain c ria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain Area de Prehisto d Unidad asociada al CSIC, Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, Calle Jos e Gutierrez Abascal, 2. 28006 Madrid, Spain e Sociedad de Ciencias Aranzadi-Aranzadi Zientzia Elkartea, Alto de Zorroaga Bidea, 11, 20014, Donostia, Gipuzkoa, Spain f Faculty of Medicine in the Galilee, Bar Ilan University, Henrietta Szold, 8, P.O.B 1589, 1311502, Zefat, Israel g Department of Radiology, Medical University Innsbruck, Anichstrasse 35, 6020 Innsbruck, Austria h n, C/ Teniente Alfonso Martínez s/n, 33011, Oviedo, Spain Department of History, University of Oviedo, Campus del Mila b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 March 2014 Accepted 17 October 2014 Available online 3 January 2015
Reconstructing the morphology of the Neanderthal rib cage not only provides information about the general evolution of human body shape but also aids understanding of functional anatomy and energetics. Despite this paleobiological importance there is still debate about the nature and extent of var n Neandertals can be used to iations in the size and shape of the Neandertal thorax. The El Sidro contribute to this debate, providing new costal remains ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs are particularly well preserved and offer the opportunity to analyze thorax morphology in Neandertals. The aims of this paper are to present this new material, to compare the ontogenetic trajectories of the first ribs between Neandertals and modern humans, and, using geometric morphometrics, to test the hypothesis of morphological integration between the first rib n adult Neandertals are smaller in centroid and overall thorax morphology. The first ribs of the El Sidro size and tend to be less curved when compared with those of modern humans, but are similar to Kebara 2. Our results further show that the straightening of the first ribs is significantly correlated with a straightening of the ribs of the upper thorax (R ¼ 0.66; p < 0.0001) in modern humans, suggesting modularity in the upper and lower thorax units as reported in other hominins. It also supports the hypothesis that the upper thorax of Neandertals differs in shape from modern humans with more anteriorly projecting upper ribs during inspiration. These differences could have biomechanical consequences and account for stronger muscle attachments in Neandertals. Different upper thorax shape would also imply a different spatial arrangement of the shoulder girdle and articulation with the humerus (torsion) and its connection to the upper thorax. Future research should address these inferences in the context of Neandertal overall body morphology. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Costal skeleton Body shape Integration Semilandmarks Homo neanderthalensis
Introduction Hypotheses about the paleobiological significance of Neandertal thorax morphology have referred to different factors ranging from
* Corresponding author. E-mail address: [email protected] (M. Bastir). http://dx.doi.org/10.1016/j.jhevol.2014.10.008 0047-2484/© 2014 Elsevier Ltd. All rights reserved.
cold adaptations, energetics and activity levels, and increased body mass (Franciscus and Churchill, 2002; Churchill, 2006) to questions related to the evolution of overall body shape (Jellema et al., 1993; mez-Olivencia et al., 2009; García-Martínez Ruff, 2002, 2010; Go et al., 2012; Bastir et al., 2013a,b). Despite its importance, the extent of differences in the size and shape of the Neandertal thorax is still not entirely clear (Franciscus and Churchill, 2002; Churchill, mez-Olivencia et al., 2009). The question of size and shape 2006; Go
M. Bastir et al. / Journal of Human Evolution 80 (2015) 64e73
differences is also important in the light of recent evidence that supports a division of the thorax into an upper and a lower part for functional, developmental and evolutionary reasons in different hominin species (Arensburg, 1991; Schmid et al., 2013; Bastir et al., 2013b, in press). While the upper part (ribs 1e5) has been related to thoracic breathing and to upper limb locomotion, the lower part (ribs 6e12) reflects features related to diaphragmatic breathing, posture and body shape as well as sub-thoracic organ content (Bastir et al., 2013b). In a pioneering quantitative analysis of isolated ribs of the Shanidar 3 Neandertal, Franciscus and Churchill (2002) suggested that the lower Neandertal thorax is larger in volume with more rounded cross sections of the lower ribs than in modern humans. Other researchers have suggested that the ribs of the lower thorax mez-Olivencia et al., 2009; in Kebara 2 are relatively large (Go García Martínez et al., 2014a). This evidence, together with a complete reconstruction of a Neandertal skeleton (Sawyer and Maley, 2005) suggests a wider lower thorax in Neandertals than in modern humans. The morphology of the upper thorax in Neandertals is considerably less well known. Sizes of the upper ribs of Kebara 2 seem to be all within or at the lower end of the range of modern humans mez-Olivencia et al., 2009; García Martínez et al., 2014a). (Go However, there is also evidence suggesting that the shape might be different. Karl Gorjanovi c-Kramberger (1906) described the first ribs of the Krapina Neandertals as particularly straight, much less curved than those of modern humans. Straightness of the first ribs in other Neandertals has also been observed in subsequent work mez(McCown and Keith, 1939; Franciscus and Churchill, 2002; Go Olivencia et al., 2009). Based on his observations of the first ribs, Gorjanovi c-Kramberger (1906) further speculated that the entire rib cage of the Krapina Neandertals probably projected more anteriorly than in modern humans (“wodurch auch der Brustkorb €lbt war”; Gorjanovic-Kramberger, 1906: 212). Thus, mehr vorgewo by predicting that the morphology of the first rib is significantly correlated to the shape of the remaining thorax, Gorjanovi cKramberger (1906) proposed an important hypothesis that is relevant to the previously mentioned studies on general thorax morphology and evolution (Franciscus and Churchill, 2002; mez-Olivencia et al., 2009). Go Anatomically, Gorjanovi c-Kramberger's (1906) hypothesis is related to the fact that the upper ribs of the thorax share an intimate relation with the respiratory system and are mutually connected by the intercostal muscles and the costo-sternal cartilages to form the chest wall (De Troyer et al., 2005). These soft-tissue connections and the need for coordinated function during lung ventilation (Franciscus and Churchill, 2002; West, 2012) probably account for the integration of the superior ribs into a morphofunctional upper thoracic unit that has been reported in different hominin species (Schmid et al., 2013; Bastir et al., 2013b). These anatomical and morphological observations justify the assumption of rib covariation patterns in modern humans and Neandertals. However, the hypothesis of Gorjanovi c-Kramberger (1906) has not yet been tested. The scantiness of upper thorax elements (for example, first ribs) in the Neandertal fossil record as well as the difficulty in properly quantifying the curved morphology of the outer rib circumference have thus far hampered a thorough analysis of this important problem. n Neandertal site in Asturias, northern Spain (Fortea The El Sidro et al., 2003; Rosas et al., 2006, 2012), which to date has produced the largest sample of Neandertal fossils in the Iberian Peninsula, also provides a significant contribution to the fossil record of thoracic elements. In addition, geometric morphometrics of 3D landmarks can be used for rigorous quantification of rib curvature, which is a key factor of overall thoracic morphology and variation
65
(García-Martínez et al., 2012, 2013; Bastir et al., 2013b). When combining geometric morphometrics and partial least squares (PLS) analysis, it is also possible to quantify and visualize shape covariation of two different anatomical systems (Rohlf and Corti, 2000; Bastir et al., 2005), such as the first rib and the remaining thorax. Thus, the aim of the present study is to describe and analyze n Neandertals within the framework a set of first ribs of the El Sidro of Gorjanovic-Kramberger's (1906) hypothesis that the morphology of the first rib morphology is significantly related to the shape of the remaining skeletal thorax. Material and methods n (Asturias, Spain) has produced a The fossil site of El Sidro considerable sample of thoracic elements, ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs SD-417, SD-1225, SD-1699 þ SD-1685 (two fragments fitted together, termed SD-1699þ onwards), SD-1767, SD-2148, SD-2172, are particularly well preserved (Fig. 1; Table 1). The ribs, like n site (Rosas et al., 2006; Bastir most of the fossils from the El Sidro et al., 2010) were covered to a variable degree with calcite concretions as a result of being embedded in the sedimentary matrix (Rosas et al., 2006, 2011). Prior to analyses, these concretions were mechanically removed to facilitate the best possible observation of ndez surface details of the bones for anatomical description (Ferna n et al., 2010). Casco Once the concretions had been removed, morphological descriptions and linear measurements (Tables 2 and 3) were under n rib fossils. The comparative sample taken for the original El Sidro included linear measurements of high quality casts of earlier Homo [KNM-WT 15000 (African Homo erectus or Homo ergaster), ATD6108, Homo antecessor] and 3D reconstructions of CT scans of the first ribs of Kebara 2 (Arensburg, 1991) and of La Ferrassie VI, a Neandertal child of approximately three to five years of age (Heim, 1982; Tompkins and Trinkaus, 1987). These data, and data taken from the literature, were compared with measurements on 3D reconstructions of CT scans of a growth series of isolated first ribs of 27 modern humans ranging from newborns to adults of both sexes, including infants (0e3 years), children (
