Few studies have directly compared human and African ape upper limb skeletal asymmetries despite the potential such comparisons have for understanding the origins of functional lateralization in humans and non-human primates. Here, we report the magnitude and direction of asymmetries in humeral torsion and humeral length in paired humeri of 40 Gorilla gorilla, 40 Pan troglodytes and 40 Homo sapiens. We test whether absolute and directional asymmetries differ between measurements, species and sexes. Our results show that humans are unique in being lateralized to the right for both measurements, consistent with human population-level handedness patterns, while apes show no significant directionality at the species level in either measurement. However, absolute torsion asymmetries in apes occur in the same magnitude as in humans, suggesting the existence of functional lateralization at the individual level.

Keywords:
Humeral length, Humeral torsion, Absolute asymmetry, Directional asymmetry, African apes
1.
Arcadi A, Wallauer W (2011). Individual-level lateralization in the asymmetrical gaits of wild chimpanzees (Pan troglodytes): implications for hand preference and skeletal asymmetry? Behaviour 148: 1419-1441.
2.
Auerbach BM, Raxter MH (2008). Patterns of clavicular bilateral asymmetry in relation to the humerus: variation among humans. Journal of Human Evolution 54: 663-674.
3.
Auerbach BM, Ruff CB (2006). Limb bone bilateral asymmetry: variability and commonality among modern humans. Journal of Human Evolution 50: 203-218.
4.
Bareggi R, Grill V, Zweyer M, Sandrucci MA, Narducci P, Forabosco A (1994). The growth of long bones in human embryological and fetal upper limbs and its relationship to other developmental patterns. Anatomy and Embryology 189: 19-24.
5.
Blackburn A (2011). Bilateral asymmetry of the humerus during growth and development. American Journal of Physical Anthropology 145: 639-646.
6.
Byrne R, Byrne J (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. beringei). Cortex 27: 521-546.
7.
Byrne RW (2004). Sex difference in chimpanzee handedness. American Journal of Physical Anthropology 123: 62-68.
8.
Carlson KJ (2006). Muscle architecture of the common chimpanzee (Pan troglodytes): perspectives for investigating chimpanzee behavior. Primates 47: 218-229.
9.
Cashmore L (2009). Can hominin ‘handedness' be accurately assessed? Annals of Human Biology 36: 624-641.
10.
Cashmore L, Zakrzewski SR (2011). Assessment of musculoskeletal stress marker development in the hand. International Journal of Osteoarchaeology 47: 218-229.
11.
Cashmore L, Uomini N, Chapelain A (2008). The evolution of handedness in humans and great apes: a review and current issues. Journal of Anthropological Sciences Rivista di Antropologia JASS Instituto Italiano di Antropologia 86: 7-35.
12.
Churchill SE, Formicola V (1997). A case of marked bilateral asymmetry in the upper limbs of an Upper Palaeolithic male from Barma Grande (Liguria), Italy. International Journal of Osteoarchaeology 7: 18-38.
13.
Codine P, Bernard PL, Pocholle M, Benaim C, Brun V (1997). Influence of sports discipline on shoulder rotator cuff balance. Medicine and Science in Sports and Exercise 29: 1400-1405.
14.
Corballis MC (2003). From mouth to hand: gesture, speech, and the evolution of right-handedness. Behavioral and Brain Sciences 26: 199-208.
15.
Cowgill LW (2007). Humeral torsion revisited: a functional and ontogenetic model for populational variation. American Journal of Physical Anthropology 134: 472-480.
16.
Crockett HC, Gross LB, Wilk KE, Schwartz ML, Reed J, O'Mara J, Reilly MT, Dugas JR, Meister K, Lyman S (2002). Osseous adaptation and range of motion at the glenohumeral joint in professional baseball pitchers. The American Journal of Sports Medicine 30: 20-26.
17.
Doran DM (1993). Sex differences in adult chimpanzee positional behavior: the influence of body size on locomotion and posture. American Journal of Physical Anthropology 91: 99-115.
18.
Drapeau MSM (2008). Enthesis bilateral asymmetry in humans and African apes. Journal of Comparative Human Biology 59: 93-109.
19.
Edelson G (1999). Variations in the retroversion of the humeral head. Journal of Shoulder and Elbow Surgery 8: 142-145.
20.
Edelson G (2000). The development of humeral head retroversion. Journal of Shoulder and Elbow Surgery 9: 316-318.
21.
Evans FG, Krahl VE (1945). The torsion of the humerus: a phylogenetic survey from fish to man. American Journal of Anatomy 76: 303-337.
22.
Fatah A, El Hak E, Shirley NR, Mahfouz MR, Auerbach BM (2012). A three-dimensional analysis of bilateral directional asymmetry in the human clavicle. American Journal of Physical Anthropology 149: 547-559.
23.
Gjerdrum T, Walker P, Andrushko V (2003). Humeral retroversion: an activity pattern index in prehistoric southern California. American Journal of Physical Anthropology 34(suppl): 100-101.
24.
Hepper PG, McCartney GR, Shannon EA (1998). Lateralised behaviour in first trimester human foetuses. Neuropsychologia 36: 531-534.
25.
Hildebrand M (1967). Symmetrical gaits of primates. American Journal of Physical Anthropology 26: 119-130.
26.
Hopkins WD, Cantalupo C (2004). Handedness in chimpanzees (Pan troglodytes) is associated with asymmetries of the primary motor cortex but not with homologous language areas. Behavioral Neuroscience 118: 1176.
27.
Hopkins WD, Cantalupo C (2005). Individual and setting differences in the hand preferences of chimpanzees (Pan troglodytes): a critical analysis and some alternative explanations. Laterality: Asymmetries of Body, Brain, and Cognition 10: 65-80.
28.
Hopkins WD, Nir TM (2010). Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): the effect of handedness and comparison with findings in humans. Behavioural Brain Research 208: 436-443.
29.
Hopkins WD, Bard KA, Griner KM (1997). Locomotor adaptation and leading limb asymmetries in neonatal chimpanzees (Pan troglodytes). International Journal of Primatology 18: 105-114.
30.
Hopkins WD, Russell JL, Cantalupo C (2007). Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes). Psychological Science 18: 971.
31.
Hopkins WD, Phillips KA, Bania A, Calcutt SE, Gardner M, Russell J, Schaeffer J, Lonsdorf EV, Ross SR, Schapiro SJ (2011). Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in Hominins. Journal of Human Evolution 60: 605- 611.
32.
Humle T, Matsuzawa T (2009). Laterality in hand use across four tool-use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa. American Journal of Primatology 71: 40-48.
33.
Hunt KD (1994). The evolution of human bipedality: ecology and functional morphology. Journal of Human Evolution 26: 183-202.
34.
Jolicoeur P (1963). Bilateral symmetry and asymmetry in limb bones of Martes americana and man. Revue Canadienne de Biologie/Editée par l'Université de Montréal 22: 409.
35.
Kontulainen S, Sievnen H, Kannus P, Pasanen M, Vuori I (2002). Effect of long-term impact of loading on mass, size, and estimated strength of humerus and radius of female racquet sports players: a peripheral quantitative computed tomography study between young and old starters and controls. Journal of Bone and Mineral Research 17: 2281-2289.
36.
Krahl VE (1976). The phylogeny and ontogeny of humeral torsion. American Journal of Physical Anthropology 45: 595-599.
37.
Larson SG (2007). Evolutionary transformation of the hominin shoulder. Evolutionary Anthropology: Issues, News, and Reviews 16: 172-187.
38.
Larson SG, Stern JT (1987). EMG of chimpanzee shoulder muscles during knuckle walking: problems of terrestrial locomotion in a suspensory adapted primate. Journal of Zoology 212: 629-655.
39.
Latimer HB, Lowrance E (1965). Bilateral asymmetry in weight and in length of human bones. The Anatomical Record 152: 217-224.
40.
Lazenby RA (2002). Skeletal biology, functional asymmetry and the origins of ‘handedness'. Journal of Theoretical Biology 218: 129-138.
41.
Lazenby RA, Cooper DM, Angus S, Hallgrímsson B (2008). Articular constraint, handedness, and directional asymmetry in the human second metacarpal. Journal of Human Evolution 54: 875- 885.
42.
Lieberman DE, Polk JD, Demes B (2003). Predicting long bone loading from cross sectional geometry. American Journal of Physical Anthropology 123: 156-171.
43.
Llorente M, Riba D, Palou L, Carrasco L, Mosquera M, Colell M, Feliu O (2011). Population level right handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 animals from Zambia and Spain. American Journal of Primatology 73: 281-290.
44.
Lonsdorf EV, Hopkins WD (2005). Wild chimpanzees show population-level handedness for tool use. Proceedings of the National Academy of Sciences of the United States of America 102: 12634-12638.
45.
Mair SD, Uhl TL, Robbe RG, Brindle KA (2004). Physeal changes and range-of-motion differences in the dominant shoulders of skeletally immature baseball players. Journal of Shoulder and Elbow Surgery 13: 487-491.
46.
Manning J, Chamberlain A (1991). Left-side cradling and brain lateralization. Ethology and Sociobiology 12: 237-244.
47.
Manning J, Heaton R, Chamberlain A (1994). Left-side cradling: similarities and differences between apes and humans. Journal of Human Evolution 26: 77-83.
48.
Marchant L, McGrew W (1991). Laterality of function in apes: a meta-analysis of methods. Journal of Human Evolution 21: 425-438.
49.
Marchant L, McGrew W (1996). Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities. Journal of Human Evolution 30: 427-443.
50.
Marchant L, McGrew W (2007). Ant fishing by wild chimpanzees is not lateralised. Primates 48: 22-26.
51.
Marchi D (2007). Relative strength of the tibia and fibula and locomotor behavior in hominoids. Journal of Human Evolution 53: 647-655.
52.
Marchi D (2008). Relationships between lower limb cross sectional geometry and mobility: the case of a Neolithic sample from Italy. American Journal of Physical Anthropology 137: 188-200.
53.
Martin CP (1933). The cause of torsion of the humerus and of the notch on the anterior edge of the glenoid cavity of the scapula. Journal of Anatomy 67: 572-582.
54.
Matsumura A, Gunji H, Takahashi Y, Nishida T, Okada M (2010). Cross-sectional morphology of the femoral neck of wild chimpanzees. International Journal of Primatology 31: 219-238.
55.
Matsumura A, Takahashi Y, Okada M (2002). Cross-sectional geometric properties along the diaphysis of femur and humerus in chimpanzees and humans. Zeitschrift für Morphologie und Anthropologie 83: 373-382.
56.
Mays S, Steele J, Ford M (1999). Directional asymmetry in the human clavicle. International Journal of Osteoarchaeology 9: 18-28.
57.
McGrew WC, Marchant LF (1996). On which side of the apes? Ethological study of laterality of hand use. In Great Ape Societies (McGrew WC, Marchant L, Nichida T, eds), pp 255-272. Cambridge, Cambridge University Press.
58.
McGrew WC, Marchant LF (1997). On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. American Journal of Physical Anthropology 104: 201-232.
59.
McGrew WC, Marchant LF (2001). Ethological study of manual laterality in the chimpanzees of the Mahale Mountains, Tanzania. Behaviour 138: 329-358.
60.
Meguerditchian A, Calcutt SE, Lonsdorf EV, Ross SR, Hopkins WD (2010). Brief communication: captive gorillas are right handed for bimanual feeding. American Journal of Physical Anthropology 141: 638-645.
61.
Morbeck ME, Galloway A, Zihlman AL, Mowbray KM (1994). Skeletal asymmetry and hand preference during termite fishing by Gombe chimpanzees. Primates 35: 99-103.
62.
Morcillo A, Fernandez Carriba S, Loeches A (2006). Asymmetries in postural control and locomotion in chimpanzees (Pan troglodytes). American Journal of Primatology 68: 802-811.
63.
Murachovsky J, Ikemoto RY, Nascimento LGP, Bueno RS, Strose E, Almeida LH (2010). Does the presence of proximal humerus growth plate changes in young baseball pitchers happen only in symptomatic athletes? An X-ray evaluation of 21 young baseball pitchers. British Journal of Sports Medicine 44: 90-94.
64.
Myers JB, Oyama S, Goerger BM, Rucinski TJ, Blackburn JT, Creighton RA (2009). Influence of humeral torsion on interpretation of posterior shoulder tightness measures in overhead athletes. Clinical Journal of Sport Medicine 19: 366-371.
65.
Osbahr DC, Cannon DL, Speer KP (2002). Retroversion of the humerus in the throwing shoulder of college baseball pitchers. The American Journal of Sports Medicine 30: 347-353.
66.
Pande B, Singh I (1971). One-sided dominance in the upper limbs of human fetuses as evidenced by asymmetry in muscle and bone weight. Journal of Anatomy 109: 457-459.
67.
Parnell RJ (2001). Hand preference for food processing in wild western lowland gorillas (Gorilla gorilla gorilla). Journal of Comparative Psychology 115: 365-375.
68.
Pearson O, Cordero R, Busby A (2006). How different were Neanderthals' habitual activities? A comparative analysis with diverse groups of recent humans. In Neanderthals Revisited: New Approaches and Perspectives (Harvati K, Harrison T, eds), pp 135-156. Dordrecht, Springer.
69.
Pieper HG (1998). Humeral torsion in the throwing arm of handball players. The American Journal of Sports Medicine 26: 247-253.
70.
Porac C, Coren S (1981). Lateral Preferences and Human Behavior. New York, Springer.
71.
Pouydebat E, Reghem E, Gorce P, Bels V (2010). Influence of the task on hand preference: individual differences among gorillas (Gorilla gorilla gorilla). Folia Primatologica 81: 273-281.
72.
Pöyhiä TH, Nietosvaara YA, Remes VM, Kirjavainen MO, Peltonen JI, Lamminen AE (2005). MRI of rotator cuff muscle atrophy in relation to glenohumeral joint incongruence in brachial plexus birth injury. Pediatric Radiology 35: 402-409.
73.
Pritchett JW (1991). Growth plate activity in the upper extremity. Clinical Orthopaedics and Related Research 268: 235-242.
74.
R Development Core Team (2010). R: A Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing.
75.
Raymond M, Pontier D (2004). Is there geographical variation in human handedness? Laterality: Asymmetries of Body, Brain and Cognition 9: 35-51.
76.
Remis M (1995). Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic. American Journal of Physical Anthropology 97: 413-433.
77.
Rhodes JA (2006). Adaptations to humeral torsion in medieval Britain. American Journal of Physical Anthropology 130: 160-166.
78.
Rhodes JA, Churchill SE (2009). Throwing in the Middle and Upper Paleolithic: inferences from an analysis of humeral retroversion. Journal of Human Evolution 56: 1-10.
79.
Rhodes JA, Knüsel CJ (2005). Activity-related skeletal change in medieval humeri: cross-sectional and architectural alterations. American Journal of Physical Anthropology 128: 536-546.
80.
Roy TA, Ruff CB, Plato CC (1994). Hand dominance and bilateral asymmetry in the structure of the second metacarpal. American Journal of Physical Anthropology 94: 203-211.
81.
Ruff C (1987). Sexual dimorphism in human lower limb bone structure: relationship to subsistence strategy and sexual division of labor. Journal of Human Evolution 16: 391-416.
82.
Ruff C (1990). Body mass and hindlimb bone cross-sectional and articular dimensions in anthropoid primates. In Body Size in Mammalian Paleobiology: Estimation and Biological Implications (Damuth J, McFadden BJ, eds), pp 119-149. Cambridge, Cambridge University Press.
83.
Ruff CB (2003). Long bone articular and diaphyseal structure in Old World monkeys and apes. II. Estimation of body mass. American Journal of Physical Anthropology 120: 16-37.
84.
Ruff CB, Hayes WC (1983). Cross-sectional geometry of Pecos Pueblo femora and tibiae - a biomechanical investigation. II. Sex, age, and side differences. American Journal of Physical Anthropology 60: 383-400.
85.
Ruff CB, Trinkaus E, Walker A, Larsen CS (1993). Postcranial robusticity in Homo. I. Temporal trends and mechanical interpretation. American Journal of Physical Anthropology 91: 21-53.
86.
Sarringhaus L, Stock J, Marchant L, McGrew W (2005). Bilateral asymmetry in the limb bones of the chimpanzee (Pan troglodytes). American Journal of Physical Anthropology 128: 840-845.
87.
Schwab LM, Blanch P (2009). Humeral torsion and passive shoulder range in elite volleyball players. Physical Therapy in Sport 10: 51-56.
88.
Schultz AH (1937). Proportions, variability and asymmetries of the long bones of the limbs and the clavicles in man and apes. Human Biology 9: 281-328.
89.
Shaw CN (2011). Is hand preference ‘coded' in the hominin skeleton? An in-vivo study of bilateral morphological variation. Journal of Human Evolution 61: 480-487.
90.
Shaw CN, Hofmann CL, Petraglia MD, Stock JT, Gottschall JS (2012). Neandertal humeri may reflect adaptation to scraping tasks, but not spear thrusting. PLoS One 7: e40349.
91.
Shaw CN, Stock JT (2009a). Habitual throwing and swimming correspond with upper limb diaphyseal strength and shape in modern human athletes. American Journal of Physical Anthropology 140: 160-172.
92.
Shaw CN, Stock JT (2009b). Intensity, repetitiveness, and directionality of habitual adolescent mobility patterns influence the tibial diaphysis morphology of athletes. American Journal of Physical Anthropology 140: 149-159.
93.
Shaw CN, Stock JT (2011). The influence of body proportions on femoral and tibial midshaft shape in hunter-gatherers. American Journal of Physical Anthropology 144: 22-29.
94.
Sherwood CC, Wahl E, Erwin JM, Hof PR, Hopkins WD (2007). Histological asymmetries of primary motor cortex predict handedness in chimpanzees (Pan troglodytes). The Journal of Comparative Neurology 503: 525-537.
95.
Sladek V, Berner M, Sosna D, Sailer R (2007). Human manipulative behavior in the central European late Neolithic and early bronze age: humeral bilateral asymmetry. American Journal of Physical Anthropology 133: 669-681.
96.
Smaers JB, Mulvaney PI, Soligo C, Zilles K, Amunts K (2012). Sexual dimorphism and laterality in the evolution of the primate prefrontal cortex. Brain, Behavior and Evolution 79: 205-212.
97.
Steele J (2000a). Handedness in past human populations: skeletal markers. Laterality: Asymmetries of Body, Brain and Cognition 5: 193-220.
98.
Steele J (2000b). Skeletal indicators of handedness. In Human Osteology (Cox M, Mays S, eds.), pp 307-323. London, Greenwich Medical Media.
99.
Steele J, Mays S (1995). Handedness and directional asymmetry in the long bones of the human upper limb. International Journal of Osteoarchaeology 5: 39-49.
100.
Stirland A (1993). Asymmetry and activity, age-related change in the male humerus. International Journal of Osteoarchaeology 3: 105-113.
101.
Stock J, Pfeiffer S (2001). Linking structural variability in long bone diaphyses to habitual behaviors: foragers from the southern African Later Stone Age and the Andaman Islands. American Journal of Physical Anthropology 115: 337-348.
102.
Stock JT, Pfeiffer SK (2004). Long bone robusticity and subsistence behaviour among Later Stone Age foragers of the forest and fynbos biomes of South Africa. Journal of Archaeological Science 31: 999-1013.
103.
Stout D, Chaminade T (2012). Stone tools, language and the brain in human evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 75-87.
104.
Taylor R, Zheng C, Jackson R, Doll J, Chen J, Holzbaur K, Besier T, Kuhl E. (2009). The phenomenon of twisted growth: humeral torsion in dominant arms of high performance tennis players. Computer Methods in Biomechanics and Biomedical Engineering 12: 83-93.
105.
Thomas SJ, Swanik CB, Kaminski TW, Higginson JS, Swanik KA, Bartolozzi AR, Nazarian LN (2012). Humeral retroversion and its association with posterior capsule thickness in collegiate baseball players. Journal of Shoulder and Elbow Surgery 21: 910-916.
106.
Trinkaus E, Churchill SE, Ruff CB (1994). Postcranial robusticity in Homo. II. Humeral bilateral asymmetry and bone plasticity. American Journal of Physical Anthropology 93: 1-34.
107.
Van Der Sluijs JA, Van Ouwerkerk WJR, De Gast A, Wuisman P, Nollet F, Manoliu RA (2002). Retroversion of the humeral head in children with an obstetric brachial plexus lesion. Journal of Bone & Joint Surgery, British Volume 84: 583-587.
108.
Vilensky JA, Larson SG (1989). Primate locomotion: utilization and control of symmetrical gaits. Annual Review of Anthropology 18: 17-35.
109.
Warton D, Duursma R, Falster D, Taskinen S (2011). Smatr: (standardized) major axis estimation and testing routines. R package version 3.2.3. http://CRAN.R-project.org/package=smatr.
110.
Waters PM, Smith GM, Jaramillo D (1998). Glenohumeral deformity secondary to brachial birth palsy. Journal of Bone & Joint Surgery, American Volume 80: 668-676.
111.
Weiss E (2009). Sex differences in humeral bilateral asymmetry in two hunter-gatherer populations: California Amerinds and British Columbian Amerinds. American Journal of Physical Anthropology 140: 19-24.
112.
White TD, Black MT, Folkens PA (2011). Human Osteology. San Diego, Academic Press.
113.
Whiteley R, Adams R, Nicholson L, Ginn K (2008). Shoulder proprioception is associated with humeral torsion in adolescent baseball players. Physical Therapy in Sport 9: 177-184.
114.
Whiteley R, Adams R, Ginn K, Nicholson L (2010). Playing level achieved, throwing history, and humeral torsion in Masters baseball players. Journal of Sports Sciences 28: 1223-1232.
115.
Wyland DJ, Pill SG, Shanley E, Clark J, Hawkins RJ, Noonan TJ, Kissenberth MJ, Thigpen CA (2012). Bony adaptation of the proximal humerus and glenoid correlate within the throwing shoulder of professional baseball pitchers. The American Journal of Sports Medicine 40: 1858-1862.
116.
Wilcox RR (2001). Fundamentals of Modern Statistical Methods: Substantially Improving Power and Accuracy. New York, Springer.
© 2013 S. Karger AG, Basel
2013
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.