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Modern or distinct axial bauplan in early hominins? A reply to Williams (2012)
Journal of Human Evolution 63 (2012) 557e559
Contents lists available at SciVerse ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
News and views
Modern or distinct axial bauplan in early hominins? A reply to Williams (2012) Martin Haeusler a, b, c, *, Schiess Regula b, Boeni Thomas a, c a
Centre for Evolutionary Medicine, Institute of Anatomy, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland Anthropological Institute and Museum, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland c Orthopaedic University Hospital Balgrist, Forchstrasse 340, 8008 Zuerich, Switzerland b
a r t i c l e i n f o Article history: Received 15 March 2012 Accepted 8 May 2012 Available online 29 June 2012 Keywords: Early hominids Vertebral column Axial skeleton Facet joint orientation
In our recent paper, we provided new evidence on the segmentation of the vertebral column of Plio-Pleistocene hominins (Haeusler et al., 2011). We presented additional vertebral and rib fragments of KNM-WT 15000, confirming our earlier suspicion that this specimen had 12 thoracic and five lumbar elements as is modal in modern humans, rather than six lumbar elements (Haeusler et al., 2002). Moreover, due to the absence of a previously suggested additional element between T11 (KNM-WT 15000 Y) and the vertebra now identified as T12 (KNM-WT 15000 AR/BA), there are only six segments with dorsomedially oriented (‘lumbar-type’) superior articular facets rather than seven as was previously believed. While these findings are not contested by Williams (2012a), he rightly points out that now in all three known fossil hominin vertebral columns (i.e., KNM-WT 15000, Sts 14 and Stw 431) the superior articular facets change their orientation from dorsomedial to dorsolateral at T11. A fourth early hominin fossil listed by Williams (2012a), MH2 (Australopithecus sediba) from Malapa, has been only preliminarily described so far. According to Berger et al. (2010), it includes three lower thoracic but no lumbar vertebrae. Williams (2012b) specifies that the facet joint orientation changes at the penultimate rib-bearing vertebra. However, due to the absence of the lumbar spine, it is not possible to unambiguously determine in this specimen the level of the transitional vertebra. Hence, the question remains whether there is sufficient evidence to * Corresponding author. Centre for Evolutionary Medicine, Anatomical Institute, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland. E-mail address: [email protected] (M. Haeusler). 0047-2484/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jhevol.2012.05.011
allow distinction of the three early hominins Sts 14, Stw 431 and KNM-WT 15000 from modern humans with respect to the position of the transitional vertebra (less fittingly termed ‘diaphragmatic vertebra’ by Williams, 2011; see Haeusler et al., 2002). Central to this issue is the location where this change in orientation of the facet joints takes place in modern humans. According to White and Panjabi (1990), the transition can be at any vertebra from T9 through L1. Anatomical textbooks report modal positions either at T11 (e.g., Gray and Standring, 2009; see also; Kazarian, 1981) or at T12 (e.g., Rauber and Kopsch, 1987). Accordingly, morphologic studies disagree about the exact prevalence of the transitional vertebra at T11. In a small sample of 37 subadult skeletons, we observed the transition in 48.6% of cases at the penultimate thoracic level, whereas our review of the literature suggested prevalence figures between 40% and 70% in different modern human populations (Lanier, 1939; Allbrook, 1955; Singer et al., 1988; Shinohara, 1997). Williams (2012a) now believes that the transition occurs with a much higher frequency at T12 and in only 26.4% of modern humans at T11. Specifically, Williams (2012a) objects that these investigations are “often hampered by different methodologies and/or lack of a formalized definition of zygapophyseal orientation change” and that we have deliberately dismissed two older studies (Hasebe, 1913; Stewart, 1932) that show a low prevalence of the transitional vertebra at T11. We partly agree with the former statement. However, since the publication of Lanier (1939), there is general agreement in the literature that a dorsomedially oriented facet joint should be classified as ‘lumbar’, and a dorsolaterally oriented
558
M. Haeusler et al. / Journal of Human Evolution 63 (2012) 557e559
one as ‘thoracic’ (e.g., Allbrook, 1955; Kazarian, 1981; Malmivaara et al., 1987; White and Panjabi, 1990; Panjabi et al., 1993; Shinohara, 1997; Masharawi et al., 2004). This orientation is equivalent to the arc of a circle, the centre of which lies either dorsal or ventral to the vertebral canal, and thus their transverse facet joint angle is either below or above 90 . Only Hasebe (1913) and Stewart (1932) and probably Williams (2011) relied on a more vague shape definition rather than the orientation of the facet joints. They considered a ‘plane Gelenkfläche’, i.e., a ‘flat’ facet joint as thoracic and a ‘transversalgebogene Gelenkfläche’ or ‘deeply curved’ one as lumbar (see Hasebe, 1913; Stewart, 1932). For this reason, we have excluded these two studies. Williams (2012a) further notes that both Hasebe (1913) and Lanier (1939) used a different vertebral counting system (postoccipital number rather than regional as in all other studies). Although we think this is of minor importance, it is perhaps better to exclude the study of Lanier (1939), too. Therefore, the lowest reported prevalence in the literature for the transitional vertebra at T11 would be 43.5% (Allbrook, 1955). On the other hand, the study of Singer et al. (1988) is noteworthy for the highest reported frequency of the transitional vertebra at T11, if those spines with gradual and abrupt changes are grouped together. Williams (2012a) criticizes this grouping because Singer et al. (1988) did not list the transverse facet angles for the individuals with a gradual change. However, their paper shows scatter plots of the transverse facet angles for the different spinal levels. We have now re-analysed these graphs. They indicate that the transition occurs in approximately 8% of the population at T10, 57% at T11, 34% at T12 and 1% at L1. Following Schultz (1930, 1961), we have attributed asymmetric transitions half to the cranial level and half to the caudal level. These revised figures suggest a slightly higher percentage of the population having the transitional vertebra at T12 or L1 than that reported by Singer et al. (1988) (35% rather than 30%). However, we did not have the original dataset at our disposal. Conversely, they also reveal a large proportion in which the transition occurs as cranial as at T10. We agree with Williams (2012a) that the limitation of Singer et al. (1988) study lies in their methodology of measuring axial CT-scans. Thus, Panjabi et al. (1993) point out that measured thoracic transverse facet angles are less and measured lumbar transverse facet angles are greater than the true angles if the vertebra is not aligned exactly in the axial plane. Only a 90 angle is not affected by an oblique alignment of the vertebra with the CTslice and thus there is theoretically no impact on the true position of the transitional vertebra. The results of Singer et al. (1988) are also supported by Davis (1955), who observed the level of transition from thoracic to lumbar type facet joints in 46 of 67 (69%) vertebral columns at T11 and in five cases (7%) at T10, although he used a slightly different definition. In addition, the study of Malmivaara (1987; cited by Panjabi et al., 1993) showed a mean transverse facet angle of 82 at the T11e12 joint, which further confirms that the 11th thoracic vertebra can be the most frequent site of transition. Masharawi et al. (2004) reported similar results. Based on 240 vertebral columns of the HamanneTodd collection, they calculated a mean transverse facet angle of 77.8 (SD 27.2 ) at the T11e12 joint. This again implies that T11 is the most common transitional vertebra in their dataset, although they did not report a frequency distribution. As they digitized 3D landmarks with a MicroScribe, it further suggests that the results of Singer et al. (1988) cannot be simply dismissed due to the measurement of CT-scans versus dry bones. In addition, Williams (2012a) criticizes the Singer et al. (1988) study because most of their data derives from abdominal CT-scans. As the upper thoracic skeleton is not represented in these CTscans, the precise segmental identification is unknown. In fact, up
to 6% of modern humans may have 13 thoracic vertebrae, whereas less than 1% has only 11 thoracic vertebrae (Hasebe, 1913; Lanier, 1939; Allbrook, 1955; Pilbeam, 2004). However, even by taking this variation of the length of the thoracic vertebral column into account, it would not change the implication of Singer et al. (1988) study that T11 is the most frequent transitional vertebra in their dataset. On the other hand, Williams (2012a) proposes to ignore all instances with asymmetric and gradual transitions of facet joint orientation. We strongly disagree with this procedure. Already in 1926, Whitney observed that asymmetries in facet joint orientation form an integrative part of the variation at the thoracolumbar border. It would certainly be better to count these facet joints as half thoracic and half lumbar. Similarly problematic is Williams’ (2012a) treatment of the individuals showing a gradual rather than abrupt change in the orientation of the facet joints. A gradual transition has been observed in between 34% (Shinohara, 1997), 54% (Singer et al., 1988) and up to 93% (Pal and Routal, 1999) of the analysed populations, but based on the above definition it is clear that any facet joint with a transverse facet joint angle below 90 should be classified as lumbar. Therefore, we do not accept Williams’ (2012a) liberal re-interpretation of these datasets where he removed all instances with asymmetric and gradual transitions of facet joint orientation and pooled them with the incompatible studies of Hasebe (1913) and Stewart (1932). Our reassessment corroborates that between 43% (Allbrook, 1955) and well over 60% (Singer et al., 1988) of modern humans show a placement of the transitional vertebra at T11. Thus, the configuration of the early hominin spines conforms to a substantial proportion of the modern human population. Consequently, the statistical arguments put forward by Williams (2012a) do not allow a distinction to be made between early hominins and modern humans with respect to this trait. This could of course change if the complete lumbar column of MH2 (A. sediba) is found and further fossil vertebral columns are discovered. Therefore, the functional significance of the position of the transitional vertebra in early hominins remains elusive. Yet, the null hypothesis of no difference in function of the lumbar spine between early hominins and modern humans cannot be rejected based on the available three fossils. References Allbrook, D.B., 1955. The East African vertebral column. Am. J. Phys. Anthropol. 13, 489e514. Berger, L.R., de Ruiter, D.J., Churchill, S.E., Schmid, P., Carlson, K.J., Dirks, P.H., Kibii, J.M., 2010. Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 328, 195e204. Davis, P.R., 1955. The thoraco-lumbar mortice joint. J. Anat. 89, 370e377. Gray, H., Standring, S., 2009. Gray’s Anatomy: The Anatomical Basis of Clinical Practice, 40th ed. Churchill Livingstone, Edinburgh. Haeusler, M., Martelli, S., Boeni, T., 2002. Vertebrae numbers of the early hominid lumbar spine. J. Hum. Evol. 43, 621e643. Haeusler, M., Schiess, R., Boeni, T., 2011. New vertebral and rib material point to modern bauplan of the Nariokotome Homo erectus skeleton. J. Hum. Evol. 61, 575e582. Hasebe, K., 1913. Die Wirbelsäule der Japaner. Z. Morphol. Anthropol. 15, 259e380. Kazarian, L., 1981. Injuries to the human spinal column: biomechanics and injury classification. Exerc. Sport Sci. Rev. 9, 297e352. Lanier, R.R., 1939. The presacral vertebrae of American white and negro males. Am. J. Phys. Anthropol. 25, 341e420. Malmivaara, A., 1987. Thoracolumbar Junctional Region of the Spine: An Anatomical, Pathological and Radiological Study. Academic Dissertation, Institute of Occupational Health, Helsinki, Finland. Malmivaara, A., Videman, T., Kuosma, E., Troup, J.D., 1987. Facet joint orientation, facet and costovertebral joint osteoarthrosis, disc degeneration, vertebral body osteophytosis, and Schmorl’s nodes in the thoracolumbar junctional region of cadaveric spines. Spine 12, 458e463. Masharawi, Y., Rothschild, B., Dar, G., Peleg, S., Robinson, D., Been, E., Hershkovitz, I., 2004. Facet orientation in the thoracolumbar spine: three-dimensional anatomic and biomechanical analysis. Spine 29, 1755e1763.
M. Haeusler et al. / Journal of Human Evolution 63 (2012) 557e559 Pal, G.P., Routal, R.V., 1999. Mechanism of change in the orientation of the articular process of the zygapophyseal joint at the thoracolumbar junction. J. Anat. 195, 199e209. Panjabi, M.M., Oxland, T., Takata, K., Goel, V., Duranceau, J., Krag, M., 1993. Articular facets of the human spine. Quantitative three-dimensional anatomy. Spine 18, 1298e1310. Pilbeam, D., 2004. The anthropoid postcranial axial skeleton: comments on development, variation, and evolution. J. Exp. Zool. 302B, 241e267. Rauber, A., Kopsch, F., 1987. Anatomie des Menschen: Lehrbuch und Atlas. Band 1: Bewegungsapparat. Thieme-Verlag, Stuttgart. Schultz, A.H., 1930. The skeleton of the trunk and limbs of higher primates. Hum. Biol. 2, 303e438. Schultz, A.H., 1961. Vertebral column and thorax. In: Hofer, H., Schultz, A.H., Starck, D. (Eds.), Primatologia, Handbuch der Primatenkunde. Karger, Basel, pp. 1e66. Shinohara, H., 1997. Changes in the surface of the superior articular joint from the lower thoracic to the upper lumbar vertebrae. J. Anat. 190, 461e465.
559
Singer, K.P., Breidahl, P.D., Day, R.E., 1988. Variations in zygapophyseal joint orientation and level of transition at the thoracolumbar junction. Preliminary survey using computed tomography. Surg. Radiol. Anat. 10, 291e295. Stewart, T.D., 1932. The vertebral column of the Eskimo. Am. J. Phys. Anthropol. 17, 123e136. White, A.A., Panjabi, M.M., 1990. Clinical Biomechanics of the Spine, second ed. Lippincott, Philadelphia. Whitney, T.A., 1926. Asymmetry of vertebral articular processes and facets. Am. J. Phys. Anthropol. 9, 451e455. Williams, S.A., 2011. Evolution of the hominoid vertebral column. Ph.D. Dissertation, University of Illinois at Urbana-Champaign. Williams, S.A., 2012. Modern or distinct axial bauplan in early hominins? Comments on Haeusler et al. (2011). J. Hum. Evol.. http://dx.doi.org/10.1016/ j.jhevol.2012.1001.1007 Williams, S.A., 2012. Placement of the diaphragmatic vertebra in catarrhines: implications for the evolution of dorsostability in hominoids and bipedalism in hominins. Am. J. Phys. Anthropol. 148, 111e122.
Contents lists available at SciVerse ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
News and views
Modern or distinct axial bauplan in early hominins? A reply to Williams (2012) Martin Haeusler a, b, c, *, Schiess Regula b, Boeni Thomas a, c a
Centre for Evolutionary Medicine, Institute of Anatomy, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland Anthropological Institute and Museum, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland c Orthopaedic University Hospital Balgrist, Forchstrasse 340, 8008 Zuerich, Switzerland b
a r t i c l e i n f o Article history: Received 15 March 2012 Accepted 8 May 2012 Available online 29 June 2012 Keywords: Early hominids Vertebral column Axial skeleton Facet joint orientation
In our recent paper, we provided new evidence on the segmentation of the vertebral column of Plio-Pleistocene hominins (Haeusler et al., 2011). We presented additional vertebral and rib fragments of KNM-WT 15000, confirming our earlier suspicion that this specimen had 12 thoracic and five lumbar elements as is modal in modern humans, rather than six lumbar elements (Haeusler et al., 2002). Moreover, due to the absence of a previously suggested additional element between T11 (KNM-WT 15000 Y) and the vertebra now identified as T12 (KNM-WT 15000 AR/BA), there are only six segments with dorsomedially oriented (‘lumbar-type’) superior articular facets rather than seven as was previously believed. While these findings are not contested by Williams (2012a), he rightly points out that now in all three known fossil hominin vertebral columns (i.e., KNM-WT 15000, Sts 14 and Stw 431) the superior articular facets change their orientation from dorsomedial to dorsolateral at T11. A fourth early hominin fossil listed by Williams (2012a), MH2 (Australopithecus sediba) from Malapa, has been only preliminarily described so far. According to Berger et al. (2010), it includes three lower thoracic but no lumbar vertebrae. Williams (2012b) specifies that the facet joint orientation changes at the penultimate rib-bearing vertebra. However, due to the absence of the lumbar spine, it is not possible to unambiguously determine in this specimen the level of the transitional vertebra. Hence, the question remains whether there is sufficient evidence to * Corresponding author. Centre for Evolutionary Medicine, Anatomical Institute, University of Zuerich, Winterthurerstrasse 190, 8057 Zuerich, Switzerland. E-mail address: [email protected] (M. Haeusler). 0047-2484/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jhevol.2012.05.011
allow distinction of the three early hominins Sts 14, Stw 431 and KNM-WT 15000 from modern humans with respect to the position of the transitional vertebra (less fittingly termed ‘diaphragmatic vertebra’ by Williams, 2011; see Haeusler et al., 2002). Central to this issue is the location where this change in orientation of the facet joints takes place in modern humans. According to White and Panjabi (1990), the transition can be at any vertebra from T9 through L1. Anatomical textbooks report modal positions either at T11 (e.g., Gray and Standring, 2009; see also; Kazarian, 1981) or at T12 (e.g., Rauber and Kopsch, 1987). Accordingly, morphologic studies disagree about the exact prevalence of the transitional vertebra at T11. In a small sample of 37 subadult skeletons, we observed the transition in 48.6% of cases at the penultimate thoracic level, whereas our review of the literature suggested prevalence figures between 40% and 70% in different modern human populations (Lanier, 1939; Allbrook, 1955; Singer et al., 1988; Shinohara, 1997). Williams (2012a) now believes that the transition occurs with a much higher frequency at T12 and in only 26.4% of modern humans at T11. Specifically, Williams (2012a) objects that these investigations are “often hampered by different methodologies and/or lack of a formalized definition of zygapophyseal orientation change” and that we have deliberately dismissed two older studies (Hasebe, 1913; Stewart, 1932) that show a low prevalence of the transitional vertebra at T11. We partly agree with the former statement. However, since the publication of Lanier (1939), there is general agreement in the literature that a dorsomedially oriented facet joint should be classified as ‘lumbar’, and a dorsolaterally oriented
558
M. Haeusler et al. / Journal of Human Evolution 63 (2012) 557e559
one as ‘thoracic’ (e.g., Allbrook, 1955; Kazarian, 1981; Malmivaara et al., 1987; White and Panjabi, 1990; Panjabi et al., 1993; Shinohara, 1997; Masharawi et al., 2004). This orientation is equivalent to the arc of a circle, the centre of which lies either dorsal or ventral to the vertebral canal, and thus their transverse facet joint angle is either below or above 90 . Only Hasebe (1913) and Stewart (1932) and probably Williams (2011) relied on a more vague shape definition rather than the orientation of the facet joints. They considered a ‘plane Gelenkfläche’, i.e., a ‘flat’ facet joint as thoracic and a ‘transversalgebogene Gelenkfläche’ or ‘deeply curved’ one as lumbar (see Hasebe, 1913; Stewart, 1932). For this reason, we have excluded these two studies. Williams (2012a) further notes that both Hasebe (1913) and Lanier (1939) used a different vertebral counting system (postoccipital number rather than regional as in all other studies). Although we think this is of minor importance, it is perhaps better to exclude the study of Lanier (1939), too. Therefore, the lowest reported prevalence in the literature for the transitional vertebra at T11 would be 43.5% (Allbrook, 1955). On the other hand, the study of Singer et al. (1988) is noteworthy for the highest reported frequency of the transitional vertebra at T11, if those spines with gradual and abrupt changes are grouped together. Williams (2012a) criticizes this grouping because Singer et al. (1988) did not list the transverse facet angles for the individuals with a gradual change. However, their paper shows scatter plots of the transverse facet angles for the different spinal levels. We have now re-analysed these graphs. They indicate that the transition occurs in approximately 8% of the population at T10, 57% at T11, 34% at T12 and 1% at L1. Following Schultz (1930, 1961), we have attributed asymmetric transitions half to the cranial level and half to the caudal level. These revised figures suggest a slightly higher percentage of the population having the transitional vertebra at T12 or L1 than that reported by Singer et al. (1988) (35% rather than 30%). However, we did not have the original dataset at our disposal. Conversely, they also reveal a large proportion in which the transition occurs as cranial as at T10. We agree with Williams (2012a) that the limitation of Singer et al. (1988) study lies in their methodology of measuring axial CT-scans. Thus, Panjabi et al. (1993) point out that measured thoracic transverse facet angles are less and measured lumbar transverse facet angles are greater than the true angles if the vertebra is not aligned exactly in the axial plane. Only a 90 angle is not affected by an oblique alignment of the vertebra with the CTslice and thus there is theoretically no impact on the true position of the transitional vertebra. The results of Singer et al. (1988) are also supported by Davis (1955), who observed the level of transition from thoracic to lumbar type facet joints in 46 of 67 (69%) vertebral columns at T11 and in five cases (7%) at T10, although he used a slightly different definition. In addition, the study of Malmivaara (1987; cited by Panjabi et al., 1993) showed a mean transverse facet angle of 82 at the T11e12 joint, which further confirms that the 11th thoracic vertebra can be the most frequent site of transition. Masharawi et al. (2004) reported similar results. Based on 240 vertebral columns of the HamanneTodd collection, they calculated a mean transverse facet angle of 77.8 (SD 27.2 ) at the T11e12 joint. This again implies that T11 is the most common transitional vertebra in their dataset, although they did not report a frequency distribution. As they digitized 3D landmarks with a MicroScribe, it further suggests that the results of Singer et al. (1988) cannot be simply dismissed due to the measurement of CT-scans versus dry bones. In addition, Williams (2012a) criticizes the Singer et al. (1988) study because most of their data derives from abdominal CT-scans. As the upper thoracic skeleton is not represented in these CTscans, the precise segmental identification is unknown. In fact, up
to 6% of modern humans may have 13 thoracic vertebrae, whereas less than 1% has only 11 thoracic vertebrae (Hasebe, 1913; Lanier, 1939; Allbrook, 1955; Pilbeam, 2004). However, even by taking this variation of the length of the thoracic vertebral column into account, it would not change the implication of Singer et al. (1988) study that T11 is the most frequent transitional vertebra in their dataset. On the other hand, Williams (2012a) proposes to ignore all instances with asymmetric and gradual transitions of facet joint orientation. We strongly disagree with this procedure. Already in 1926, Whitney observed that asymmetries in facet joint orientation form an integrative part of the variation at the thoracolumbar border. It would certainly be better to count these facet joints as half thoracic and half lumbar. Similarly problematic is Williams’ (2012a) treatment of the individuals showing a gradual rather than abrupt change in the orientation of the facet joints. A gradual transition has been observed in between 34% (Shinohara, 1997), 54% (Singer et al., 1988) and up to 93% (Pal and Routal, 1999) of the analysed populations, but based on the above definition it is clear that any facet joint with a transverse facet joint angle below 90 should be classified as lumbar. Therefore, we do not accept Williams’ (2012a) liberal re-interpretation of these datasets where he removed all instances with asymmetric and gradual transitions of facet joint orientation and pooled them with the incompatible studies of Hasebe (1913) and Stewart (1932). Our reassessment corroborates that between 43% (Allbrook, 1955) and well over 60% (Singer et al., 1988) of modern humans show a placement of the transitional vertebra at T11. Thus, the configuration of the early hominin spines conforms to a substantial proportion of the modern human population. Consequently, the statistical arguments put forward by Williams (2012a) do not allow a distinction to be made between early hominins and modern humans with respect to this trait. This could of course change if the complete lumbar column of MH2 (A. sediba) is found and further fossil vertebral columns are discovered. Therefore, the functional significance of the position of the transitional vertebra in early hominins remains elusive. Yet, the null hypothesis of no difference in function of the lumbar spine between early hominins and modern humans cannot be rejected based on the available three fossils. References Allbrook, D.B., 1955. The East African vertebral column. Am. J. Phys. Anthropol. 13, 489e514. Berger, L.R., de Ruiter, D.J., Churchill, S.E., Schmid, P., Carlson, K.J., Dirks, P.H., Kibii, J.M., 2010. Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 328, 195e204. Davis, P.R., 1955. The thoraco-lumbar mortice joint. J. Anat. 89, 370e377. Gray, H., Standring, S., 2009. Gray’s Anatomy: The Anatomical Basis of Clinical Practice, 40th ed. Churchill Livingstone, Edinburgh. Haeusler, M., Martelli, S., Boeni, T., 2002. Vertebrae numbers of the early hominid lumbar spine. J. Hum. Evol. 43, 621e643. Haeusler, M., Schiess, R., Boeni, T., 2011. New vertebral and rib material point to modern bauplan of the Nariokotome Homo erectus skeleton. J. Hum. Evol. 61, 575e582. Hasebe, K., 1913. Die Wirbelsäule der Japaner. Z. Morphol. Anthropol. 15, 259e380. Kazarian, L., 1981. Injuries to the human spinal column: biomechanics and injury classification. Exerc. Sport Sci. Rev. 9, 297e352. Lanier, R.R., 1939. The presacral vertebrae of American white and negro males. Am. J. Phys. Anthropol. 25, 341e420. Malmivaara, A., 1987. Thoracolumbar Junctional Region of the Spine: An Anatomical, Pathological and Radiological Study. Academic Dissertation, Institute of Occupational Health, Helsinki, Finland. Malmivaara, A., Videman, T., Kuosma, E., Troup, J.D., 1987. Facet joint orientation, facet and costovertebral joint osteoarthrosis, disc degeneration, vertebral body osteophytosis, and Schmorl’s nodes in the thoracolumbar junctional region of cadaveric spines. Spine 12, 458e463. Masharawi, Y., Rothschild, B., Dar, G., Peleg, S., Robinson, D., Been, E., Hershkovitz, I., 2004. Facet orientation in the thoracolumbar spine: three-dimensional anatomic and biomechanical analysis. Spine 29, 1755e1763.
M. Haeusler et al. / Journal of Human Evolution 63 (2012) 557e559 Pal, G.P., Routal, R.V., 1999. Mechanism of change in the orientation of the articular process of the zygapophyseal joint at the thoracolumbar junction. J. Anat. 195, 199e209. Panjabi, M.M., Oxland, T., Takata, K., Goel, V., Duranceau, J., Krag, M., 1993. Articular facets of the human spine. Quantitative three-dimensional anatomy. Spine 18, 1298e1310. Pilbeam, D., 2004. The anthropoid postcranial axial skeleton: comments on development, variation, and evolution. J. Exp. Zool. 302B, 241e267. Rauber, A., Kopsch, F., 1987. Anatomie des Menschen: Lehrbuch und Atlas. Band 1: Bewegungsapparat. Thieme-Verlag, Stuttgart. Schultz, A.H., 1930. The skeleton of the trunk and limbs of higher primates. Hum. Biol. 2, 303e438. Schultz, A.H., 1961. Vertebral column and thorax. In: Hofer, H., Schultz, A.H., Starck, D. (Eds.), Primatologia, Handbuch der Primatenkunde. Karger, Basel, pp. 1e66. Shinohara, H., 1997. Changes in the surface of the superior articular joint from the lower thoracic to the upper lumbar vertebrae. J. Anat. 190, 461e465.
559
Singer, K.P., Breidahl, P.D., Day, R.E., 1988. Variations in zygapophyseal joint orientation and level of transition at the thoracolumbar junction. Preliminary survey using computed tomography. Surg. Radiol. Anat. 10, 291e295. Stewart, T.D., 1932. The vertebral column of the Eskimo. Am. J. Phys. Anthropol. 17, 123e136. White, A.A., Panjabi, M.M., 1990. Clinical Biomechanics of the Spine, second ed. Lippincott, Philadelphia. Whitney, T.A., 1926. Asymmetry of vertebral articular processes and facets. Am. J. Phys. Anthropol. 9, 451e455. Williams, S.A., 2011. Evolution of the hominoid vertebral column. Ph.D. Dissertation, University of Illinois at Urbana-Champaign. Williams, S.A., 2012. Modern or distinct axial bauplan in early hominins? Comments on Haeusler et al. (2011). J. Hum. Evol.. http://dx.doi.org/10.1016/ j.jhevol.2012.1001.1007 Williams, S.A., 2012. Placement of the diaphragmatic vertebra in catarrhines: implications for the evolution of dorsostability in hominoids and bipedalism in hominins. Am. J. Phys. Anthropol. 148, 111e122.