Was Australopithecus afarensis able to make the Lomekwian stone tools? Towards a realistic biomechanical simulation of hand force capability in fossil hominins and new insights on the role of the fifth digit

Abstract While no consensus allows explaining how and when human-like traits arose in fossil hominin hands, the recent discoveries of the Lomekwian stone tools (3.3 Ma) support the view that early hominins were able to use forceful grips in order to manipulate large-sized blocks for pounding activities. Then, assessing gripping abilities of contemporaneous hominin, i.e. Australopithecus afarensis, is necessary, particularly with regards to its unusual 5th ray morphology that has been deemed crucial to ensure forceful grips. Here, we present a musculoskeletal simulation based on the A. afarensis hand morphology that includes an original 5th carpometacarpal joint. Our first results suggest a limited influence of muscle parameters (e.g., PCSA) and support the value of simulations for studying extinct taxa even in absence of soft-tissue data. Given the inability for the pulp of the 5th ray to face the surface of a large-sized object, the A. afarensis hand would have had limited possibility to exert sufficient force to make the Lomekwian stone tools.

[1]  S. Churchill,et al.  Australopithecus sediba Hand Demonstrates Mosaic Evolution of Locomotor and Manipulative Abilities , 2011, Science.

[2]  M. Drapeau Metacarpal torsion in apes, humans, and early Australopithecus: implications for manipulatory abilities , 2015, PeerJ.

[3]  Zong-Ming Li,et al.  Biomechanical effect of increasing or decreasing degrees of freedom for surgery of trapeziometacarpal joint arthritis: A simulation study , 2011, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[4]  Jie Tang,et al.  Coordination of thumb joints during opposition. , 2007, Journal of biomechanics.

[5]  R. Lieber,et al.  Architecture of selected muscles of the arm and forearm: anatomy and implications for tendon transfer. , 1992, The Journal of hand surgery.

[6]  D. McFadden,et al.  Sex differences in the relative lengths of metacarpals and metatarsals in gorillas and chimpanzees , 2005, Hormones and Behavior.

[7]  Benjamin J. Majors,et al.  Development and Validation of a Computational Model for Investigation of Wrist Biomechanics , 2011, Annals of Biomedical Engineering.

[8]  K. An,et al.  Tendon excursion and moment arm of index finger muscles. , 1983, Journal of biomechanics.

[9]  Dieter H. Pahr,et al.  Human-like hand use in Australopithecus africanus , 2015, Science.

[10]  F. J. Alonso,et al.  A comparison among different Hill-type contraction dynamics formulations for muscle force estimation , 2016 .

[11]  M W Marzke,et al.  Functional capabilities of modern and fossil hominid hands: three-dimensional analysis of trapezia. , 2003, American journal of physical anthropology.

[12]  Akinori Nagano,et al.  Neuromusculoskeletal computer modeling and simulation of upright, straight-legged, bipedal locomotion of Australopithecus afarensis (A.L. 288-1). , 2005, American journal of physical anthropology.

[13]  Rui Diogo,et al.  Evolution and homologies of primate and modern human hand and forearm muscles, with notes on thumb movements and tool use. , 2012, Journal of human evolution.

[14]  R. Lieber,et al.  Architectural design of the human intrinsic hand muscles. , 1992, The Journal of hand surgery.

[15]  K N An,et al.  Normative model of human hand for biomechanical analysis. , 1979, Journal of biomechanics.

[16]  Carol V Ward,et al.  New postcranial fossils of Australopithecus afarensis from Hadar, Ethiopia (1990-2007). , 2012, Journal of human evolution.

[17]  Eric Berton,et al.  Comparison of tendon tensions estimated from two biomechanical models of the thumb. , 2009, Journal of biomechanics.

[18]  C. Marean,et al.  Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia , 2010, Nature.

[19]  D. Jindrich,et al.  Finger Muscle Attachments for an OpenSim Upper-Extremity Model , 2015, PloS one.

[20]  Mary W Marzke,et al.  Tool making, hand morphology and fossil hominins , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  Christopher J Dunmore,et al.  The evolution of the hominin thumb and the influence exerted by the non-dominant hand during stone tool production. , 2015, Journal of human evolution.

[22]  Scott W Wolfe,et al.  Studying Primate Carpal Kinematics in Three Dimensions Using a Computed‐Tomography‐Based Markerless Registration Method , 2010, Anatomical record.

[23]  Brian G Richmond,et al.  Hand pressure distribution during Oldowan stone tool production. , 2012, Journal of human evolution.

[24]  R. L. Susman Hand function and tool behavior in early hominids. , 1998, Journal of human evolution.

[25]  Daniel E Lieberman,et al.  The coevolution of human hands and feet. , 2010, Evolution; international journal of organic evolution.

[26]  B. Richmond,et al.  Upper limb kinematics and the role of the wrist during stone tool production. , 2010, American journal of physical anthropology.

[27]  Edmund Y. S. Chao,et al.  Biomechanics of the hand : a basic research study , 1989 .

[28]  B. Richmond,et al.  Biomechanical strategies for accuracy and force generation during stone tool production. , 2014, Journal of human evolution.

[29]  L. M. Myers,et al.  The axes of rotation of the thumb carpometacarpal joint , 1992, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[30]  Anand A Joshi,et al.  Global point signature for shape analysis of carpal bones , 2014, Physics in medicine and biology.

[31]  R H Tuttle,et al.  Quantitative and functional studies on the hands of the anthropoidea. I. The Hominoidea , 1969, Journal of morphology.

[32]  J. T. Stern,et al.  The locomotor anatomy of Australopithecus afarensis. , 1983, American journal of physical anthropology.

[33]  R. Crompton,et al.  Inertial properties of hominoid limb segments , 2006, Journal of anatomy.

[34]  F. V. D. van der Helm,et al.  The effect of scaling physiological cross-sectional area on musculoskeletal model predictions. , 2015, Journal of biomechanics.

[35]  E. Berton,et al.  Effect of object width on muscle and joint forces during thumb-index finger grasping. , 2011, Journal of applied biomechanics.

[36]  M. Domínguez‐Rodrigo,et al.  Configurational approach to identifying the earliest hominin butchers , 2010, Proceedings of the National Academy of Sciences.

[37]  H. Roche,et al.  3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya , 2015, Nature.

[38]  V M Zatsiorsky,et al.  The effect of finger extensor mechanism on the flexor force during isometric tasks. , 2001, Journal of biomechanics.

[39]  Christophe Boesch,et al.  Different hand postures for pounding nuts with natural hammers by wild chimpanzees , 1993 .

[40]  C. Rolian,et al.  Reassessing manual proportions in Australopithecus afarensis. , 2013, American journal of physical anthropology.

[41]  D. Grimaud-Hervé,et al.  Carpal kinematics in quadrupedal monkeys: towards a better understanding of wrist morphology and function , 2012, Journal of anatomy.

[42]  C. Ward,et al.  Forelimb segment length proportions in extant hominoids and Australopithecus afarensis. , 2007, American journal of physical anthropology.

[43]  Franck Multon,et al.  From bone to plausible bipedal locomotion. Part II: Complete motion synthesis for bipedal primates. , 2009, Journal of biomechanics.

[44]  C. Lovejoy,et al.  Hominid tarsal, metatarsal, and phalangeal bones recovered from the Hadar Formation: 1974-1977 collections , 1982 .

[45]  M. Taieb,et al.  Pliocene hominids from the Hadar formation, Ethiopia (1973–1977): Stratigraphic, chronologic, and paleoenvironmental contexts, with notes on hominid morphology and systematics , 1982 .

[46]  S. Moyà-Solà,et al.  Morphological affinities of the Australopithecus afarensis hand on the basis of manual proportions and relative thumb length. , 2003, Journal of human evolution.

[47]  Benedikt Hallgrímsson,et al.  THE COEVOLUTION OF HUMAN HANDS AND FEET , 2010, Evolution; international journal of organic evolution.

[48]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[49]  R. L. Linscheid,et al.  EMG study of hand muscle recruitment during hard hammer percussion manufacture of Oldowan tools. , 1998, American journal of physical anthropology.

[50]  Jessica C. Thompson,et al.  Taphonomy of fossils from the hominin-bearing deposits at Dikika, Ethiopia. , 2015, Journal of human evolution.

[51]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

[52]  M. Marzke,et al.  Hominid hand use in the pliocene and pleistocene: Evidence from experimental archaeology and comparative morphology* , 1986 .

[53]  Sergio Almécija,et al.  On manual proportions and pad-to-pad precision grasping in Australopithecus afarensis. , 2014, Journal of human evolution.

[54]  John R Hutchinson,et al.  Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa , 2004, Journal of morphology.

[55]  Naomichi Ogihara,et al.  Muscle dimensions in the chimpanzee hand , 2005, Primates.

[56]  R M Patterson,et al.  Three-dimensional kinematic analysis of the second through fifth carpometacarpal joints. , 2001, The Journal of hand surgery.

[57]  Vladimir M Zatsiorsky,et al.  Optimization-Based Models of Muscle Coordination , 2002, Exercise and sport sciences reviews.

[58]  D. E. Ricklan,et al.  Functional anatomy of the hand of Australopithecus africanus , 1987 .

[59]  W. Sellers,et al.  Comparison of inverse-dynamics musculo-skeletal models of AL 288-1 Australopithecus afarensis and KNM-WT 15000 Homo ergaster to modern humans, with implications for the evolution of bipedalism. , 2004, Journal of human evolution.

[60]  Laurent Vigouroux,et al.  Handle Shape Affects the Grip Force Distribution and the Muscle Loadings During Power Grip Tasks. , 2015, Journal of applied biomechanics.

[61]  M. Batmanabane,et al.  Movements at the carpometacarpal and metacarpophalangeal joints of the hand and their effect on the dimensions of the articular ends of the metacarpal bones , 1985, The Anatomical record.

[62]  Daniel E Lieberman,et al.  Hand biomechanics during simulated stone tool use. , 2011, Journal of human evolution.

[63]  William L. Jungers,et al.  The evolution of human and ape hand proportions , 2015, Nature Communications.

[64]  Ajay Seth,et al.  Is my model good enough? Best practices for verification and validation of musculoskeletal models and simulations of movement. , 2015, Journal of biomechanical engineering.

[65]  D J Giurintano,et al.  A 3D biomechanical model of the hand for power grip. , 2003, Journal of biomechanical engineering.

[66]  David Bendahan,et al.  Quantification of finger joint loadings using musculoskeletal modelling clarifies mechanical risk factors of hand osteoarthritis. , 2014, Medical engineering & physics.

[67]  F E Zajac,et al.  How musculotendon architecture and joint geometry affect the capacity of muscles to move and exert force on objects: a review with application to arm and forearm tendon transfer design. , 1992, The Journal of hand surgery.

[68]  Zong-Ming Li,et al.  Three-dimensional stiffness of the carpal arch. , 2016, Journal of biomechanics.

[69]  S. Almécija,et al.  Early Origin for Human-Like Precision Grasping: A Comparative Study of Pollical Distal Phalanges in Fossil Hominins , 2010, PloS one.

[70]  Eric Berton,et al.  Determination of passive moment-angle relationships at the trapeziometacarpal joint. , 2010, Journal of biomechanical engineering.

[71]  Mary W. Marzke,et al.  Joint functions and grips of the Australopithecus afarensis hand, with special reference to the region of the capitate , 1983 .

[72]  Mary W. Marzke,et al.  Chimpanzee and human grips: A new classification with a focus on evolutionary morphology , 1996, International Journal of Primatology.

[73]  Joseph D. Towles,et al.  Towards a realistic biomechanical model of the thumb: the choice of kinematic description may be more critical than the solution method or the variability/uncertainty of musculoskeletal parameters. , 2003, Journal of biomechanics.

[74]  Y. Rak,et al.  Associated cranial and forelimb remains attributed to Australopithecus afarensis from Hadar, Ethiopia. , 2005, Journal of human evolution.

[75]  Scott L. Delp,et al.  A Model of the Upper Extremity for Simulating Musculoskeletal Surgery and Analyzing Neuromuscular Control , 2005, Annals of Biomedical Engineering.

[76]  Eric Berton,et al.  Quantification of hand and forearm muscle forces during a maximal power grip task. , 2012, Medicine and science in sports and exercise.

[77]  H. E. J. Veeger,et al.  Anatomical parameters for musculoskeletal modeling of the hand and wrist , 2016 .