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The evolution of human forelimb structure is connected with changes in patterns of human behavior. Two complementary approaches—phylogenetic and functional—are used to analyze and understand these connections.
The evolution of human forelimb structure is connected with changes in patterns of human behavior. Two complementary approaches—phylogenetic and functional—are used to analyze and understand these connections.
The human forelimb is a mosaic of morphological features that reflect the evolutionary history of locomotor and manipulative behaviors. The phylogenetic approach identifies traits shared with and derived from other species. First, the general sequence of appearance of these features can be traced through a comparative process in which traits shared with other living and fossil species are identified. Some are shared exclusively with the closest relatives of humans, the chimpanzees, indicating their relatively recent appearance, whereas others, for example, the forelimb pattern of the humerus, radius, and ulna, are found among mammals, reptiles, amphibians, and certain fossil fish, indicating that the first appearance of the feature was in a common ancestor approximately 380 million years ago. Second, features unique to humans, termed derived features (indicating that they evolved following the divergence of humans from chimpanzees 6 to 7 million years ago) can be analyzed in order to construct a cladogram, or phylogenetic tree, with nodes representing hypothetical common ancestors of humans and living and fossil nonhuman groups, inferred from the shared elements of the human mosaic pattern (Fig. 1). These groups are increasingly inclusive toward the base of the cladogram; human-derived features evolved after node 6.
The functional analytic approach involves linking the morphology of shared and derived traits to behavior. Evolutionary change in limb morphology occurred as locomotor and manipulative behaviors accommodated to changes in the ecology of successive groups of ancestral species. Functional changes in joint-movement capabilities and bone mechanics associated with morphological developments in turn facilitated the new behaviors. Tracing the evolution of human forelimb functions and behaviors has increasingly been aided by two developments: (1) new experimental approaches to the analysis of links between morphology and mechanical function1-3, and (2) evidence from developmental genetics, indicating how morphological adaptations to locomotor and manipulative behaviors may have evolved4-6. Specific hypotheses explain changes in morphological features as adaptations to changing behaviors, and investigations of convergent morphologies in distantly related species occupying similar environments also explain adaptations of forelimb functions to shared behaviors1,3,7.
Combined use of both phylogenetic and functional approaches allows investigators to reconstruct the following brief history of forelimb evolution, including the sequence of appearance and locomotor and/or manipulative functions of morphological complexes.
Humerus, Radius, Ulna, and Carpals (Fig. 1, Nodes 1 and 2)
The earliest evidence for the human forelimb pattern of the humerus, radius, and ulna appears in a fossil fish, Eusthenopteron, 380 million years ago, followed 375 million years ago by the appearance of carpal bones in the fossil species, Tiktaalik roseae. The Tiktaalik fossil forelimb is described by Shubin8, who also directed research on genes involved in the development of the upper limb. Shubin recovered the Tiktaalik fossils from the deposit of a shallow river, which may explain why fins were becoming transformed into limbs that were able to propel the animal along the substrate. This pattern has been preserved in the amphibians, reptiles, and mammals that evolved from the ancient ancestor that gave rise to Tiktaalik and to them.
Grasping Hands with Divergent Thumb, Nails, and Functional Differentiation of Forelimb from Hindlimb (Fig. 1, Node 3)
By 56 million years ago, the ancestor common to humans and prosimian primates was arboreal, feeding with the hands on fruit and insects from slender branches. Investigations of morphological and functional convergence between living prosimians and marsupials that occupy the same niche support a hypothesis that the grasping hands and feet with nails (at first, only on the hallux) are adaptations to maintaining balance on fine branches1 and, similarly, that a reduction of forelimb (relative to hindlimb) support and propulsion reflect greater emphasis on forelimb manipulative behaviors2.
Opposable Thumb (Fig. 1, Node 4)
A saddle joint between the trapezium and first metacarpal is found in humans and apes, and also in living Old World monkeys9, with which apes and humans share a common ancestor at 23 million years ago10. This joint facilitates opposition of the thumb to all finger pads in humans and to at least the index finger pad in the other species.
Mobile Shoulder, Elbow, and Wrist (Fig. 1, Node 5)
Humans share with great apes (Asian orangutans and African chimpanzees and gorillas) a pattern of forelimb joint mobility that allows the apes to suspend the body below flexible branches in the upper and outer canopy of the forest by the hands or by hand-foot combinations, as well as to pivot around the hand in reaching for fruits and handholds. Comparisons of great apes with gibbons and large-bodied New World monkey species that also are suspensory have revealed a complex of features at the forelimb joints that are adapted to suspensory postures and locomotion. Elements of this complex are retained in humans11, including large range of motion of the shoulder, full supination of the forearm, and independence of the ulna from the carpal bones. This last feature enhances ulnar deviation.
Fused Os Centrale (Fig. 1, Node 6)
In both humans and chimpanzees, the os centrale is fused with the scaphoid; these bones are separate in most other mammals. It has been suggested that this feature stabilizes the wrist for knuckle-walking, and its existence reflects knuckle-walking in the ancestor common to humans and chimpanzees12. Orr et al., using two approaches, recently found evidence in the wrist to support this hypothesis7,13. First, Orr compared wrist morphology in chimpanzees and the giant anteater, which both walk on their knuckles with the metacarpals aligned with the forearm, and found that the os centrale is fused to the scaphoid in both genera7. To test a hypothesis that this fusion provides essential stabilization to the midcarpal region during knuckle-walking, Orr et al. performed a kinematic analysis of os centrale movements in the orangutan, a non-knuckle-walking species that is closely related to the chimpanzee and that lacks os centrale fusion with the scaphoid13. They found movement of the os centrale on the scaphoid in the orangutan, leading to the inference that its fusion in knuckle-walkers reduces midcarpal mobility and enhances stability.
Hand function-morphology relationships are also seen in derived features of the human forelimb. Drapeau14 and Larson et al.15 recently analyzed the evolution of the function of the human elbow and shoulder. The following discussion focuses on the human hand and wrist features that evolved following divergence from chimpanzees.
In modern humans, a morphological complex of several skeletal and muscle features on the radial side of the wrist has been discerned and quantified through comparative dissections, kinematic analyses, and three-dimensional studies of joint surface topography (Table I)16. Additional features on the ulnar side of the modern human wrist have been observed qualitatively in comparative dissections (Table I)17. It has long been assumed that these features evolved in adaptation to human manufacture and use of tools18-21. Experiments conducted to discern links between tool-making behaviors, hand mechanics, and morphology can test this hypothesis in the laboratory. Humans can also be compared with chimpanzees to determine whether similar links between manipulative behaviors and morphology exist in both species.
Derived features of the human hand appeared around the same time as the evolution of prehistoric stone tools and were all in place before the proliferation of modern tools. Electromyographic studies of wrist and hand muscles and synchronized videotapes of grips during the replication of early stone tool use have determined the grips and hand movements that would be required for effective manufacture and use of the tools22,23. These studies indicated that three key capabilities facilitate control of the tools. First is the ability to cup the hand, enabling it to accommodate the varied shapes of the stones, bones, and wood tools21. This allows the hand to maintain control of the tools against large external forces, such as those generated by striking stone cores with hammerstones and by pounding with hammerstones and digging sticks. Cupping is facilitated by the distinctive human metacarpal base and head shapes that allow metacarpal convergence with metacarpophalangeal flexion and by the large range of opposition of the thumb metacarpal on the relatively flat trapezial surface. The second capability is the use of forceful precision grips (Table II) by the thumb and finger pads, which maintain control of stones while exposing the working edges for flake removal or food extraction and preparation. The third capability is the squeeze form of power grip (Table II), in which a cylindrical tool (e.g., a clawed hammer) is held diagonally across the palm by the thumb, fingers, and thenar and hypothenar eminences. This grip aligns the tool with the forearm, enhancing its leverage and acceleration. Substantial torque potential for maintaining these grips is provided by the significantly (p < 0.01) larger thumb muscles and tendon moment arms in humans compared with chimpanzees (Table I)24, together with the large first metacarpal belly of the first dorsal interosseous muscle16, which stabilizes the base of the thumb during movements of the phalanges25. The relatively large joint surfaces of the trapezium and scaphoid26, the significantly ( p < 0.0025) flatter topography of the trapeziometacarpal joint, and the unique shape of the human trapezoid and orientations of its facets (Fig. 2) accommodate stresses associated with muscle contraction26,27.
These three capabilities and their correlates are essential to human forelimb function; the next step is to determine whether they are unique to humans.
Cupping
Observations of chimpanzees during feeding, which requires grips exposing part of the food for biting by the teeth, indicated that two hands (occasionally supplemented by a foot with its opposable hallux) resist displacement of the food by the teeth28. Thus, in comparison with humans, chimpanzees appear to have less capable forceful precision grips as a result of a smaller force potential of thumb muscles, as well as a morphology that limits cupping of objects. Australopithecus afarensis, a small-brained hominin biped that predates the first evidence for stone tool manufacture, had proximal and distal joint configurations of the second metacarpal that allowed pronation with flexion, which is important for cupping the radial side of the hand in the three-jawed "baseball" grip that was necessary in the gripping of stones29. However, the ulnar side of the wrist does not exhibit the modern human pattern for cupping, and the joint between the trapezium and first metacarpal is strongly curved, as in chimpanzees25. Thus, an early facility for cupping the hand appears soon after the divergence of humans from the chimpanzee lineage.
Forceful Precision Grips
The first evidence for a strong thumb compatible with forceful precision grip is seen in two hominin metacarpals from Swartkrans, South Africa; these metacarpals had markings for a well-developed first metacarpal belly for the first dorsal interosseous muscle16. They are contemporary (1.75 million years ago) with stone tools and with crania that exhibit larger brain size than that of australopiths. The first fossil evidence for the modern human configuration involving the trapezoid appears in Homo antecessor26; that fossil was found in Spain and dates to 750,000 years ago. Neandertal hands at 300,000 years ago retain this pattern and are very similar to modern humans in other aspects of hand morphology, although the trapezium falls toward the outer limit of modern human variation in its low dorsovolar curvature27.
Hand morphology in Homo floresiensis (found recently on the island of Flores in Indonesia) contributes to evidence that this fossil species, despite its relatively recent age of 18,000 years ago, is a remnant of an extinct hominin species. The trapezoid complex is primitive, recalling that of chimpanzees and reflecting substantial functional differences from the modern human hand30.
Squeeze Power Grip
When chimpanzees wave cylindrical sticks in display, a transverse or oblique grip by the fingers alone is used, similar to the overhead grip of branches during suspensory feeding and locomotion. This grip differs from the power grip used by humans, as the stick is not aligned with the forearm because the palm does not cup it; therefore the chimpanzee cannot deliver a forceful blow with the stick28. Again, these differences indicate that the human hand has become uniquely adapted to the manipulation of tools, which distinguishes humans from chimpanzees.
Independent Flexor Pollicis Longus
It has been reported that 31% of humans have a connection between the flexor pollicis longus tendon and the deep flexor tendon to the index finger31, which may be associated with tenosynovitis and pain32. The relatively high occurrence of a connection in humans may be explained by the fact that the muscle is not independent of the deep finger flexors in nonhuman primates. It is possible that the frequency of connection became reduced during human evolution as forceful, repetitive pinching activities stressed the region33.
Trapeziometacarpal Arthritis
Arthritis at the trapeziometacarpal joint appears to occur more frequently in individuals with greater curvature of the mutual joint surfaces than in those with less curved surfaces34. It is not surprising then that, with the evolution of forceful and repetitive manipulation of tools, curvature became reduced in humans27. The trade-off is a tendency toward less stability at the joint than that seen in chimpanzees, with a potential for subluxation of the first metacarpal.
One of the most important findings from developmental studies is the emergence of novel morphological complexes4-6, such as those at the radial and ulnar sides of the wrist, as mentioned above. Separately, the derived human features in a complex may not be advantageous. However, individuals possessing the features of a functional morphological complex are more likely to survive and reproduce in ecological settings in which the complex is compatible and advantageous. For example, the derived features on the radial side of the hand and wrist together generate forceful grasp, orient the loads transversely from the strong thumb across the wrist, and accommodate the loads with large, relatively flat joints. Prabhaker et al. recently described a derived DNA sequence in humans that affects the development of the radial side of the wrist and the thumb in rats35, offering intriguing molecular evidence of a genetic link to the development of morphological complexes.
The human forelimb bears almost 400 million years of history in its morphology. Contrary to popular belief, the ability to oppose the thumb pad to the index finger pad is not unique to humans, but appeared approximately 23 million years ago. Some of the features and associated functions that distinguish human hands from those of other animals have not yet been the focus of clinical investigation. For example, forceful precision grips by a single hand alone, such as the three-jawed "baseball" grip, are essential to human manipulation of many objects and probably explain distinctive morphological patterns in the human hand, but they are not regularly considered in clinical discussions of precision grips.
Further kinematic and biomechanical comparative analyses of morphology in humans and in nonhuman primates will further test hypotheses of evolutionary adaptations to manipulative behaviors. Molecular genetic evidence for developmental processes of the forelimb will expand the understanding of the evolution of functional patterns of morphology. 
Lemelin P, Schmitt D. Origins of grasping and locomotor adaptations in primates: comparative and experimental approaches using an opossum model. In: Ravosa MJ, Dagosto M, editors. Primate origins: adaptations and evolution. New York: Springer; 2007. p 329-80.
2007
Larson SG. Morphological correlates of forelimb protraction in quadrupedal primates. In: Ravosa MJ, Dagosto M, editors. Primate origins: adaptations and evolution. New York: Springer; 2007. p 437-56.
2007
Dagosto M. The postcranial morphotype of primates. In: Ravosa MJ, Dagosto M, editors. Primate origins: adaptations and evolution. New York: Springer; 2007. p 489-534.
2007
Reno PL, McCollum MA, Cohn MJ, Meindl RS, Hamrick M, Lovejoy CO. Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories. J Exp Zoolog B Mol Dev Evol.2008;310:240-58.310240
2008
Hamrick MW. Evolvability, limb morphology, and primate origins. In: Ravosa MJ, Dagosto M, editors. Primate origins: adaptations and evolution. New York: Springer; 2007. p 381-402.
2007
Carroll SB. Genetics and the making of Homo sapiens. Nature.2003;422:849-57.422849
2003
[PubMed][CrossRef]
Orr CM. Knuckle-walking anteater: a convergence test of adaptation for purported knuckle-walking features of African Hominidae. Am J Phys Anthropol.2005;128:639-58.128639
2005
[CrossRef]
Shubin N. Your inner fish: a journey into the 3.5-billion-year history of the human body. New York: Pantheon Books; 2008.
2008
Rose MD. Kinematics of the trapezium-1st metacarpal joint in extant anthropoids and Miocene hominoids. J Hum Evol.1992;22:255-66.22255
1992
[CrossRef]
Glazko GV, Nei M. Estimation of divergence times for major lineages of primate species. Mol Biol Evol.2003;20:424-34.20424
2003
[CrossRef]
Larson SG. Parallel evolution in the hominoid trunk and forelimb. Evol Anthropol.1998;6:87-99.687
1998
[CrossRef]
Richmond BG, Strait DS. Evidence that humans evolved from a knuckle-walking ancestor. Nature.2000;404:382-5.404382
2000
[CrossRef]
Orr CM, Leventhal EL, Chivers FS, Crisco JJ. Kinematics of the os centrale in Pongo pygmaeus: implications for the knuckle-walking hominin ancestor hypothesis [abstract]. Am J Phys Anthropol Suppl.2008;46:166.46166
2008
Drapeau MS. Articular morphology of the proximal ulna in extant and fossil hominoids and hominins. J Hum Evol.2008;55:86-102.5586
2008
[CrossRef]
Larson SG, Jungers WL, Morwood MJ, Sutikna T, Jatmiko, Saptomo EW, Due RA, Djubiantono T. Homo floresiensis and the evolution of the hominin shoulder. J Hum Evol.2007;53:718-31.53718
2007
[CrossRef]
Tocheri MW, Orr CM, Jacofsky MC, Marzke MW. The evolutionary history of the hominin hand since the last common ancestor of Pan and Homo. J Anat.2008;212:544-62.212544
2008
[CrossRef]
Marzke MW, Wullstein KL, Viegas SF. Evolution of the power ("squeeze") grip and its morphological correlates in hominids. Am J Phys Anthropol.1992;89:283-98.89283
1992
[CrossRef]
Napier J. Fossil hand bones from Olduvai Gorge. Nature.1962;196:409-11.196409
1962
[CrossRef]
Lewis OJ. Functional morphology of the evolving hand and foot. Oxford: Oxford University Press; 1989.
1989
Susman RL. Fossil evidence for early hominid tool use. Science.1994;265:1570-3.2651570
1994
[CrossRef]
Marzke MW. Precision grips, hand morphology, and tools. Am J Phys Anthropol.1997;102:91-110.10291
1997
[CrossRef]
Marzke MW, Shackley MS. Hominid hand use in the Pliocene and Pleistocene: evidence from experimental archaeology and comparative morphology. J Hum Evol.1986;15:439-60.15439
1986
[CrossRef]
Marzke MW, Toth N, Schick K, Reece S, Steinberg B, Hunt K, Linscheid RL, An KN. EMG study of hand muscle recruitment during hard hammer percussion manufacture of Oldowan tools. Am J Phys Anthropol.1998;105:315-32.105315
1998
[CrossRef]
Marzke MW, Marzke RF, Linscheid RL, Smutz P, Steinberg B, Reece S, An KN. Chimpanzee thumb muscle cross sections, moment arms and potential torques, and comparisons with humans. Am J Phys Anthropol.1999;110:163-78.110163
1999
[CrossRef]
Brand PW, Hollister AM. Clinical mechanics of the hand. 3rd ed. St. Louis: Mosby; 1999.
1999
Tocheri MW. Three-dimensional riddles of the radial wrist: derived carpal and carpometacarpal joint morphology in the genus Homo and the implications for understanding stone tool-related behaviors in Hominins [dissertation]. Phoenix: Arizona State University; 2007.
2007
Marzke MW, Tocheri MW, Steinberg B, Femiani JD, Reece SP, Linscheid RL, Orr CM, Marzke RF. Comparative 3D quantitative analyses of trapeziometacarpal joint surface curvatures among living catarrhines and fossil hominins. Am J Phys Anthropol; submitted for publication.
Marzke MW, Wullstein KL. Chimpanzee and human grips: a new classification with a focus on evolutionary morphology. Int J Primatol.1996;17:117-39.17117
1996
[CrossRef]
Marzke MW. Joint functions and grips of the Australopithecus afarensis hand, with special reference to the region of the capitate. J Hum Evol.1983;12:197-211.12197
1983
[CrossRef]
Tocheri MW, Orr CM, Larson SG, Sutikna T, Jatmiko, Saptomo EW, Due RA, Djubiantono T, Morwood MJ, Jungers WL. The primitive wrist of Homo floresiensis and its implications for hominin evolution. Science.2007;317:1743-5.3171743
2007
[CrossRef]
Linburg RM, Comstock BE. Anomalous tendon slips from the flexor pollicis longus to the flexor digitorum profundus. J Hand Surg [Am].1979;4:79-83.479
1979
Kozin SH, Bishop AT, Cooney WP. Tendinitis of the wrist. In: Cooney WP, Linscheid RL, Dobyns JH, editors. The wrist: diagnosis and operative treatment. Vol 2. St. Louis: Mosby-Year Book; 1998. p 1181-96.
1998
Shrewsbury MM, Marzke MW, Linscheid RL, Reece SP. Comparative morphology of the pollical distal phalanx. Am J Phys Anthropol.2003;121:30-47.12130
2003
[CrossRef]
Ateshian GA, Rosenwasser MP, Mow VC. Curvature characteristics and congruence of the thumb carpometacarpal joint: differences between female and male joints. J Biomech.1992;25:591-607.25591
1992
[CrossRef]
Prabhaker S, Visel A, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Morrison H, Fitzpatrick DR, Afzal V, Pennacchio LA, Rubin EM, Noonan JP. Human-specific gain of function in a developmental enhancer. Science.2008;321:1346-50.3211346
2008
[CrossRef]