Abstract
Primates are defined, in part, by the presence of a grasping hand that couples primitive anatomy with exceptional neuromuscular dexterity. This arrangement is maintained across the evolutionary history of primates, and is often seen as one of the key features that allow primates to make fluid transitions from one substrate to another, make kinematic adjustments with changes in speed and gait, and to make biomechanical adjustments throughout ontogeny. This chapter surveys the exceptional diversity of primate hand positions across locomotor modes, and provides a perspective on the organization of hand positioning based on underlying biomechanical similarities. Across primates, hand positions are highly variable, and multiple solutions to same locomotor challenges are observed. This mechanical flexibility appears to be an adaptive feature of the primate hand, and suggests much of the success of the primate radiation has to do with maintaining generalized ‘cheiridial compromise’ that allows locomotor versatility.
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References
Almécija S, Smaers JB, Jungers WL (2015) The evolution of human and ape hand proportions. Nat Commun 6:7717
Begun DR, Kivell TL (2011) Knuckle-walking in Sivapithecus? The combined effects of homology and homoplasy with possible implications for pongine dispersals. J Hum Evol 60:158–170
Biewener AA (1983) Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. J Exp Biol 105:47–171
Biewener AA (1989) Scaling in body support in mammals: limb posture and muscle mechanics. Science 245:45–48
Bishop A (1962) Control of the hand in lower primates. N Y Acad Sci 120:316–337
Bishop A (1964) Use of the hand in lower primates. In: Buettner-Janusch J (ed) Evolutionary and genetic biology of primates. Academic Press, New York, pp 133–223
Blanchard ML, Crompton RH (2011) Field study methods for primate locomotor ecology and biomechanics. In: D’Août K, Vereecke EE (eds) Primate locomotion: linking field and laboratory research. Springer, New York, pp 183–199
Bock WJ, von Wahlert G (1965) Adaptation and the form-function complex. Evolution 19:269–299
Cant JGH, Youlatos D, Rose MD (2003) Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuni National Park, Ecuador. J Hum Evol 44:685–699
Cartmill M (1972) Arboreal adaptations and the origin of the order Primates. In: Tuttle R (ed) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago, pp 97–122
Cartmill M (1974a) Pads and claws in arboreal locomotion. In: Jenkins FA Jr (ed) Primate locomotion. Academic Press, New York, pp 45–83
Cartmill M (1985) Climbing. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge, pp 73–88
Cartmill M (1992) New views on primate origins. Evol Anthropol 1:105–111
Cartmill M, Milton K (1977) The lorisiform wrist joint and the evolution of “brachiating” adaptations in the Hominoidea. Am J Phys Anthropol 47:249–272
Charles-Dominique P, Martin RD (1970) Evolution of lorises and lemurs. Nature 227:257–260
Clevedon Brown J, Yalden DW (1973) The description of mammals—2 limbs and locomotion of terrestrial mammals. Mamm Rev 3:107–134
Congdon KA (2012) Interspecific and ontogenetic variation in proximal pedal phalangeal curvature of great apes (Gorilla gorilla, Pan troglodytes, and Pongo pygmaeus). Int J Primatol 33:418–427
Congdon KA (2014) Grasping pressures and phalangeal curvature in primates: an experimental in vivo approach. Ph.D. dissertation, University of Missouri
Day MH, Iliffe SR (1975) The contrahens muscle layer in Tarsius. Folia Primatol 24:241–249
Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467
Dietz V (2003) Spinal cord pattern generators for locomotion. Clin Neurophysiol 114:1379–1389
Doran DM (1992) The ontogeny of chimpanzee and pygmy chimpanzee locomotor behavior: a case study of paedomorphism and its behavioral correlates. J Hum Evol 23:139–157
Doran, DM (1993) Comparative locomotor behavior of chimpanzees and bonobos: the influence of morphology on locomotion. Am J Phy Anthropol, 91(1): pp.83–98.
Doran DM (1997) Ontogeny of locomotion in mountain gorillas and chimpanzees. J Hum Evol 32:323–344
Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251–261
Fleagle JG (2013) Primate adaptation and evolution, 3rd edn. Academic Press, San Diego
Foster AD, Raichlen DA, Pontzer H (2013) Muscle force production during bent-knee, bent-hip walking in humans. J Hum Evol 65:294–302
Fujiwara S, Endo H, Hutchinson JR (2011) Topsy-turvy locomotion: biomechanical specializations of the elbow in suspended quadrupeds reflect inverted gravitational constraints. J Anat 219:176–191
Gebo DL (2014) Primate comparative anatomy. Johns Hopkins University Press, Baltimore
Golubitsky M, Stewart I, Pietro-Luciano B, Collins JJ (1999) Symmetry in locomotor central pattern generators and animal gaits. Nature 401:693–695
Grand TI (1968) Functional anatomy of the upper limb. Bibl Primatol 7:104–125
Granatosky MC (2015) Kinematic and kinetic analysis of arm-swinging in the red-shanked douc langur (Pygathrix nemaeus). J Viet Primatol 2(4):33–40
Granatosky MC, Tripp CH, Schmitt D (2016) Gait kinetics of above and below branch quadrupedal locomotion in lemurid primates. J Exp Biol 219:53–63
Groves CP (1970) Gorillas. Arthur Barker, London
Guillot D (2011) Forelimb suspensory gait characteristics of wild Lagothrix poeppigii and Ateles belzebuth: developing video-based methodologies in free-ranging primates. In: D’Août K, Vereecke EE (eds) Primate locomotion: linking field and laboratory research. Springer, New York, pp 247–269
Hamrick MW, Simons EL, Jungers WL (2000) New wrist bones of the Malagasy giant subfossil lemurs. J Hum Evol 38:635–650
Hayama S, Chantani K, Nakatsukasa M (1994) The digitigrade hand and terrestrial adaptation in Japanese macaques. Anthropol Sci 102(Suppl):115–125
Heffner RS, Masterton RB (1975) Variation in form of the pyramidal tract and its relationship to digital dexterity. Brain Behav Evol 12:188–200
Hunt KD, Cant JGH, Gebo DL, Rose MD, Walker SE, Youlatos D (1996) Standardized descriptions of primate locomotor and postural modes. Primates 37:363–387
Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21:642–653
Inouye SE (1989) Variability of hand postures in the knuckle-walking behavior of African apes. Am J Phys Anthropol 78:245 (abstract)
Inouye SE (1992) Ontogeny and allometry of African ape manual rays. J Hum Evol 23:107–138
Inouye SE (1994) Ontogeny of knuckle-walking hand postures in African apes. J Hum Evol 26:459–485
Iriarte-Diaz J, Riskin DK, Breuer KS, Swartz SM (2012) Kinematic plasticity during flight in fruit bats: individual variability in response to loading. PLoS One 7:e36665
Ivanco TL, Pellis SM, Whishaw IQ (1996) Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems. Behav Brain Res 79:163–181
Iwaniuk AN, Whishaw IQ (1999) How skilled are the skilled limb movements of the raccoon (Procyon lotor)? Behav Brain Res 99(1):35–44
Jenkins FA Jr (1974) Tree shrew locomotion and the origins of primate arborealism. In: Jenkins FA Jr (ed) Primate locomotion. Academic Press, New York, pp 85–115
Jenkins FA Jr (1981) Wrist rotation in primates: a critical adaptation for brachiators. Symp Zool Soc Lond 48:429–451
Johnson LE (2012) Biomechanics of vertical clinging and grasping in primates. Ph.D. dissertation, Duke University
Johnson LE, Hanna J, Schmitt D (2015) Single-limb force data for two lemur species while vertically clinging. Am J Phys Anthropol 158:463–474
Jolly CJ (1965) The origins and specializations of long-faced Cercopithecoidea. Ph.D. dissertation, University of London
Jungers WL, Godfrey LR, Simons EL, Chatrath PS (1997) Phalangeal curvature and positional behavior in extinct sloth lemurs (Primates, Palaeopropithecidae). Proc Natl Acad Sci U S A 94:11998–20001
Kivell TL, Schmitt D (2009) Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor. Proc Natl Acad Sci U S A 106:14241–14246
Kivell TL, Schmitt D, Wunderlich RE (2010) Hand and foot pressures in the aye-aye (Daubentonia madagascariensis) reveal novel biomechanical trade-offs required for walking on gracile digits. J Exp Biol 213:1549–1557
Kivell TL, Barros AP, Smaers JB (2013) Different evolutionary pathways underlie the morphology of wrist bones in hominoids. BMC Evol Biol 13:229
Krakauer E, Lemelin P, Schmitt D (2002) Hand and body position during locomotor behavior in the aye-aye (Daubentonia madagascariensis). Am J Primatol 57(3):105–118
Larson SG, Schmitt D, Lemelin P, Hamrick MW (2001) Limb excursion during quadrupedal walking: how do primates compare to other mammals? J Zool 255:353–365
Lemelin P (1996) The evolution of manual prehensility in primates. A comparative study of prosimian primates and didelphid marsupials. Ph.D. dissertation, State University of New York at Stony Brook
Lemelin P (1999) Morphological correlates of substrate use in didelphid marsupials: implications for primate origins. J Zool 247:165–175
Lemelin P, Grafton BW (1998) Grasping performance in Saguinus midas and the evolution of hand prehensility in primates. In: Strasser E, Fleagle J, Rosenberger A, McHenry H (eds) Primate locomotion: recent advances. Plenum Press, New York, pp 131–144
Lemelin P, Schmitt D (1998) The relation between hand morphology and quadrupedalism in primates. Am J Phys Anthropol 105:185–197
Lewis OJ (1985a) Derived morphology of the wrist articulations and theories of hominoid evolution. Part II. The lorisine joints. J Anat 140:447–460
Lewis OJ (1985b) Derived morphology of the wrist articulations and theories of hominoid evolution. Part I. The midcarpal joints of higher primates. J Anat 142:151–172
MacKay-Lyons M (2002) Central pattern generation of locomotion: a review of the evidence. Phys Ther 82:69–83
Matarazzo S (2008) Knuckle walking signal in the manual digits of Pan and Gorilla. Am J Phys Anthropol 135:27–33
Matarazzo S (2013) Manual pressure distribution patterns of knuckle-walking apes. Am J Phys Anthropol 152:44–50
McClearn D (1992) Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. J Mamm 73:245–261
McClure NK, Phillips AC, Vogel ER, Tocheri MW (2012) Unexpected pollex and hallux use in wild Pongo pygmaeus wurmbii. Am J Phys Anthropol 147(Suppl 54):203 (abstract)
Meldrum DJ, Dagosto M, White J (1997) Hindlimb suspension and hind foot reversal in Varecia variegata and other arboreal mammals. Am J Phys Anthropol 103:85–102
Mendel FC (1979) The wrist joint of two-toed sloths and its relevance to brachiating adaptations in the Hominoidea. J Morphol 162:413–424
Michilsens F, Vereecke EE, D’Août K, Aerts P (2010) Muscle moment arms and function of the siamang forelimb during brachiation. J Anat 217:521–535
Mori S (1987) Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats. Prog Neurobiol 28:161–195
Mori S, Matsuyama K, Miyashita E, Nakajima K, Asanome M (1996) Basic neurophysiology of primate locomotion. Folia Primatol 66:192–203
Napier J (1962) The evolution of the hand. Sci Am 207:56–62
Napier J (1980) Hands. Pantheon Books, New York
Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, London
Napier JR, Walker AC (1967) Vertical clinging and leaping—a newly recognized category of locomotor behaviour of primates. Folia Primatol 6:204–219
Nengo O (1993) Integrating mechanical and historical approaches to organismal design: the case in the hands and feet of catarrhines. Ph.D. dissertation, Harvard University
Nieschalk U, Demes B (1993) Biomechanical determinants of reduction of the second ray in Lorisinae. In: Preuschoft H, Chivers DJ (eds) Hands of primates. Springer-Verlag, Vienna, pp 225–234
Nyakatura JA, Petrovitch A, Fischer MS (2010) Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. Zoology 113:221–234
Oxnard CE, Crompton RH, Lieberman SS (1990) Animal lifestyles and anatomies: the case of the Prosimian primates. University of Washington Press, Seattle
Patel BA (2009) Not so fast: speed effects on forelimb kinematics in cercopithecoid monkeys and implications for digitigrade postures in primates. Am J Phys Anthropol 140:92–112
Patel BA (2010a) Functional morphology of the cercopithecoid primate metacarpals. J Hum Evol 58:320–337
Patel BA (2010b) The interplay between speed, kinetics and hand postures during primate terrestrial locomotion. Am J Phys Anthropol 141:222–234
Patel BA, Polk JD (2010) Distal forelimb kinematics in Erythrocebus patas and Papio anubis during walking and galloping. Int J Primatol 31:191–207
Patel BA, Wunderlich RE (2010) Dynamic pressure patterns in the hands of olive baboons (Papio anubis) during terrestrial locomotion: implications for cercopithecoid primate hand morphology. Anat Rec 293:710–718
Patel BA, Larson SG, Stern JT Jr (2012) Electromyography of wrist and finger flexor muscles in olive baboons (Papio anubis). J Exp Biol 215:115–123
Patel BA, Horner AM, Thompson NE, Barrett L, Henzi SP (2013) Ontogenetic scaling of fore-and hind limb posture in wild chacma baboons (Papio hamadryas ursinus). PLoS One 8:e71020
Polk JD (2002) Adaptive and phylogenetic influences on musculoskeletal design in cercopithecine primates. J Exp Biol 205:3399–3412
Pontzer H, Raichlen DA, Sockol MD (2009) The metabolic cost of walking in humans, chimpanzees, and early hominins. J Hum Evol 56:43–54
Preuschoft H (2002) What does “arboreal locomotion” mean exactly and what are the relationships between “climbing”, environment and morphology? Z Morphol Anthropol 83:171–188
Rawlins RG (1993) Locomotor and manipulative use of the hand in Cayo Santiago macaques (Macaca mulatta). In: Preuschoft H, Chivers DJ (eds) Hands of primates. Springer-Verlag, Vienna, pp 21–30
Richmond BG (1997) Ontogeny of phalangeal curvature and locomotor behavior in lar gibbons. Am J Phys Anthropol 104(Suppl 24):197 (abstract)
Richmond BG (1998) Ontogeny and biomechanics of phalangeal form in primates. Ph.D. dissertation, State University of New York at Stony Brook
Richmond BG (2007) Biomechanics of phalangeal curvature. J Hum Evol 53:678–690
Richmond BG, Strait DS (2000) Evidence that humans evolved from a knuckle-walking ancestor. Nature 404:382–385
Richmond BG, Begun DR, Strait DS (2001) Origin of human bipedalism: the knuckle-walking hypothesis revisited. Yearb Phys Anthropol 44:70–105
Rollinson J, Martin RD (1981) Comparative aspects of primate locomotion, with special reference to arboreal cercopithecoids. Symp Zool Soc Lond 48:377–427
Rose MD (1973) Quadrupedalism in primates. Primates 14:337–357
Rosenberger AL, Halenar L, Cooke SB, Hartwig WC (2008) Morphology and evolution of the spider monkey, genus Ateles. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, UK, pp 19–49
Schmitt D (2010a) Translating primate locomotor biomechanical variables from the laboratory to the field. In: D’Août K, Vereecke EE (eds) Primate locomotion: linking field and laboratory research. Springer, New York, pp 7–28
Schmitt D (2010b) Primate locomotor evolution: biomechanical studies of primate locomotion and their implications for understanding primate neuroethology. In: Platt ML, Ghazanfar AA (eds) Primate neuroethology. Oxford University Press, Oxford, pp 10–30
Schmitt D, Lemelin P (2002) Origins of primate locomotion: gait mechanics of the woolly opossum. Am J Phys Anthropol 118:231–238
Schmitt D, Turnquist JE, Rose MD (2009) The relationship between arm-swinging behavior and postcranial morphology in Ateles and Lagothrix. Am J Phys Anthropol 138(Suppl 38):230 (abstract)
Soligo C, Martin RD (2006) Adaptive origins of primates revisited. J Hum Evol 50:414–430
Sockol MD, Raichlen DA, Pontzer H (2007) Chimpanzee locomotor energetics and the origin of human bipedalism. Proc Natl Acad Sci U S A 104:12265–12269
Stern JT Jr, Oxnard CE (1973) Primate locomotion: some links with evolution and morphology. Primatologia 4:1–93
Susman RL (1974) Facultative terrestrial hand postures in an orangutan (Pongo pygmaeus) and pongid evolution. Am J Phys Anthropol 40:27–37
Susman RL (1979) Comparative and functional morphology of hominoid fingers. Am J Phys Anthropol 50:215–236
Sussman RW (1991) Primate origins and the evolution of angiosperms. Am J Primatol 23:209–223
Swartz SM, Bertram JE, Biewener AA (1989) Telemetered in vivo strain analysis of locomotor mechanics of brachiating gibbons. Nature 342:270–272
Szalay FS, Dagosto M (1980) Locomotor adaptations as reflected on the humerus of Paleogene primates. Folia Primatol 34:1–45
Szalay FS, Dagosto M (1988) Evolution of hallucial grasping in the primates. J Hum Evol 17:1–33
Tripp CH, Granatosky MC, Schmitt D (2015) Forelimb mechanics during below-branch quadrupedalism in primates: a comparison to above-branch quadrupedalism and bimanual locomotion. Am J Phys Anthropol 156(Suppl 60):307 (abstract)
Tsegai ZJ, Kivell TL, Gross T, Nguyen NH, Pahr DH, Smaers JB, Skinner MM (2013) Trabecular bone structure correlates with hand posture and use in hominoids. PLoS One 8:e78781
Turnquist JE (1975) The elbow and forearm of Ateles: an anatomical and behavioral study of locomotion, Ph.D. dissertation, University of Pennsylvania
Tuttle RH (1967) Knuckle-walking and the evolution of hominoid hands. Am J Phys Anthropol 26:171–206
Tuttle RH (1969) Knuckle-walking and the problem of human origins. Science 166:953–961
Tuttle RH (1981) Evolution of hominid bipedalism and prehensile capabilities. Phil Trans R Soc Lond B292:89–94
Vilensky JA, Larson SG (1989) Primate locomotion: utilization and control of symmetrical gaits. Annu Rev Anthropol 18:17–35
Wainwright PC, Mehta RS, Higham TE (2008) Stereotypy, flexibility and coordination: key concepts in behavioral functional morphology. J Exp Biol 211:3523–3528
Weidenreich F (1931) Der primäre Greitcharacter der menschlichen Hände und Füsse und seine Bedeutung für das Abstammungsproblem. Verbandlungen Gesellschaft Phys Anthropol 5:97–110
Whitehead PF (1993) Aspects of the anthropoid wrist and hand. In: Gebo DL (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 96–102
Williams SA (2010) Morphological integration and the evolution of knuckle-walking. J Hum Evol 58:432–440
Whishaw IQ, Coles BL (1996) Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behav Brain Res 77:135–148
Whishaw IQ, Pellis SM (1990) The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component. Behav Brain Res 41:49–59
Wood Jones F (1916) Arboreal man. Edward Arnold, London
Wood Jones F (1920) The principles of anatomy as seen in the hand. J. and A. Churchill, London
Wunderlich RE, Jungers WL (2009) Manual digital pressures during knuckle-walking in chimpanzees (Pan troglodytes). Am J Phys Anthropol 139:394–403
Yalden DW (1972) The form and function of the carpal bones in some arboreally adapted mammals. Acta Anat 82:383–406
Zeininger A, Shapiro LJ, Raichlen DA (2007) Ontogeny of digitigrade hand and foot postures in baboons (Papio cynocephalus). Am J Phys Anthropol 44:255 (abstract)
Zeininger A, Shapiro LJ, Raichlen DA (2009) The effects of digitigrade cheiridial postures on speed and gait in infant baboons. Am J Phys Anthropol 138(Suppl 48):279 (abstract)
Zeininger A, Richmond BG, Hartman G (2011) Metacarpal head biomechanics: a comparative backscattered electron image analysis of trabecular bone mineral density in Pan troglodytes, Pongo pygmaeus, and Homo sapiens. J Hum Evol 60:703–710
Zeininger A, Schmitt D, Wunderlich R (2014) Developmental timing of heel-strike plantigrady in chimpanzees and gorillas. Am J Phys Anthropol 153(Suppl 58):281–282 (abstract)
Acknowledgments
A review chapter like this develops only as a result of extensive conversations with colleagues, collaborators, and friends. The topic of the evolution of the hand remains a deep and profound one in our field, and we have discussed some of the ideas here with many of our colleagues in the recent and more distant past. We thank the following people (listed in a sort of temporal order) for discussions about the ideas concerning functional anatomy of the hand presented in this chapter: Susan Larson, Jack Stern, Scott McGraw, Chris Wall, Liza Shapiro, Rich Kay, Matt Cartmill, Jean Turnquist, John Cant, Jandy Hanna, David Raichlen, Chris Vinyard, Laura Johnson, Karyne Rabey, Charlotte Miller, Steve Churchill, Doug Boyer, and Anne-Claire Fabre. We owe a special debt of gratitude to Mike Rose whose many articles on this topic and wise advice and opinions helped shape much of our thinking on hand anatomy. We are especially grateful to Pierre Lemelin, Tracy Kivell, and Brian Richmond for heavy and constructive editing of this chapter. More importantly, we are grateful to them for the many and lengthy discussions about this chapter and other issues concerning the evolution of the hand that we had over the past 3 years. Much of the data described here come from studies carried out by one or more of us at SUNY Stony Brook (laboratory of Jack Stern and Susan Larson), The University of Texas at Austin (laboratory of Jody Jensen), Monkey Jungle, and the Duke Lemur Center. We thank all the faculty and staff there in general and specifically Marianne Crisci, Sian Evans, David Brewer, Bill Hess, and Erin Ehmke.
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Schmitt, D., Zeininger, A., Granatosky, M.C. (2016). Patterns, Variability, and Flexibility of Hand Posture During Locomotion in Primates. In: Kivell, T., Lemelin, P., Richmond, B., Schmitt, D. (eds) The Evolution of the Primate Hand. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3646-5_13
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