CoChat
Sign Up
Cited by 135

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Rethinking the evolution of the human foot: insights from experimental research

Holowka, Nicholas B., Lieberman, Daniel E.·2018·Journal of Experimental Biology
DOI 10.1242/jeb.174425
Open this paper in CoChat — free account

Abstract

Adaptive explanations for modern human foot anatomy have long fascinated evolutionary biologists because of the dramatic differences between our feet and those of our closest living relatives, the great apes. Morphological features, including hallucal opposability, toe length and the longitudinal arch, have traditionally been used to dichotomize human and great ape feet as being adapted for bipedal walking and arboreal locomotion, respectively. However, recent biomechanical models of human foot function and experimental investigations of great ape locomotion have undermined this simple dichotomy. Here, we review this research, focusing on the biomechanics of foot strike, push-off and elastic energy storage in the foot, and show that humans and great apes share some underappreciated, surprising similarities in foot function, such as use of plantigrady and ability to stiffen the midfoot. We also show that several unique features of the human foot, including a spring-like longitudinal arch and short toes, are likely adaptations to long distance running. We use this framework to interpret the fossil record and argue that the human foot passed through three evolutionary stages: first, a great ape-like foot adapted for arboreal locomotion but with some adaptations for bipedal walking; second, a foot adapted for effective bipedal walking but retaining some arboreal grasping adaptations; and third, a human-like foot adapted for enhanced economy during long-distance walking and running that had lost its prehensility. Based on this scenario, we suggest that selection for bipedal running played a major role in the loss of arboreal adaptations.

Overview

Integrity signals

Registry

Crossref · 10.1242/jeb.174425

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The use of a flatter foot contact and absence of a clear heel strike may affect walking economy by reducing the total distance travelled by the body's centre of mass during a given step and/or increasing the amount of mechanical work needed to accelerate the body's centre of mass between steps.

    “The use of a flatter foot contact and absence of a clear heel strike may affect walking economy, as it may reduce the total distance travelled by the body's centre of mass during a given step (Webber & Raichlen, 2016) and/or increase the amount of mechanical work needed to accelerate the body's centre of mass between steps (Adamczyk & Kuo, 2013; Holowka & Lieberman, 2018).”

    From Forest terrains influence walking kinematics among indigenous Tsimane of the Bolivian Amazon (2022) · cites this paper as Holowka & Lieberman, 2018

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 106

  1. Adamczyk, 2013, Mechanical and energetic consequences of rolling foot shape in human walking, J. Exp. Biol., 216, 2722, 10.1242/jeb.082347 · DOI · Paper page
  2. Alexander, 1991, Energy-saving mechanisms in walking and running, J. Exp. Biol., 69, 55, 10.1242/jeb.160.1.55 · DOI
  3. Bates, 2013, The evolution of compliance in the human lateral mid-foot, Proc. R. Soc. B Biol. Sci., 280, 20131818, 10.1098/rspb.2013.1818 · DOI
  4. Behrensmeyer, 1981, Footprints of a Pleistocene hominid in northern Kenya, Nature, 289, 167, 10.1038/289167a0 · DOI
  5. Bennett, 1989, Elastic strain energy storage in the feet of running monkeys, J. Zool., 217, 469, 10.1111/j.1469-7998.1989.tb02502.x · DOI
  6. Bennett, 2009, Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenya, Science, 323, 1197, 10.1126/science.1168132 · DOI
  7. Biewener, 2004, Muscle mechanical advantage of human walking and running: implications for energy cost, J. Appl. Physiol., 97, 2266, 10.1152/japplphysiol.00003.2004 · DOI · Paper page
  8. Bojsen-Møller, 1979, Calcaneocuboid joint and stability of the longitudinal arch of the foot at high and low gear push off, J. Anat., 129, 165
  9. Bramble, 2004, Endurance running and the evolution of Homo, Nature, 432, 345, 10.1038/nature03052 · DOI
  10. Carrier, 2017, The effect of foot posture on capacity to apply free moments to the ground: implications for fighting performance in great apes, Biol. Open, 6, 269, 10.1242/bio.022640 · DOI
  11. Carrier, 1994, Variable gearing during locomotion in the human musculoskeletal system, Science, 265, 651, 10.1126/science.8036513 · DOI
  12. Cavagna, 1977, Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure, Am. J. Physiol., 233, R243
  13. Chi, 2005, Mechanical energy and effective foot mass during impact loading of walking and running, J. Biomech., 38, 1387, 10.1016/j.jbiomech.2004.06.020 · DOI
  14. Clarke, 1995, Sterkfontein member 2 foot bones of the oldest South African hominid, Science, 269, 521, 10.1126/science.7624772 · DOI
  15. Crompton, 2008, Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor, J. Anat., 212, 501, 10.1111/j.1469-7580.2008.00870.x · DOI
  16. Crompton, 2012, Human-like external function of the foot, and fully upright gait, confirmed in the 3.66 million year old Laetoli hominin footprints by topographic statistics, experimental footprint-formation and computer simulation, J. R. Soc. Interface, 9, 707, 10.1098/rsif.2011.0258 · DOI
  17. Cunningham, 2010, The influence of foot posture on the cost of transport in humans, J. Exp. Biol., 213, 790, 10.1242/jeb.038984 · DOI
  18. D'Août, 2002, Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus), Am. J. Phys. Anthropol., 119, 37, 10.1002/ajpa.10112 · DOI
  19. Day, 1964, Fossil foot bones, Nature, 201, 969, 10.1038/201969a0 · DOI
  20. Day, 1980, Laetoli Pliocene hominid footprints and bipedalism, Nature, 286, 385, 10.1038/286385a0 · DOI
  21. DeSilva, 2009, Functional morphology of the ankle and the likelihood of climbing in early hominins, Proc. Natl. Acad. Sci. USA, 106, 6567, 10.1073/pnas.0900270106 · DOI
  22. DeSilva, 2010, Revisiting the “midtarsal break”, Am. J. Phys. Anthropol., 141, 245, 10.1002/ajpa.21140 · DOI
  23. DeSilva, 2013, The lower limb and mechanics of walking in Australopithecus sediba, Science, 340, 1232999, 10.1126/science.1232999 · DOI
  24. DeSilva, 2015, Midtarsal break variation in modern humans: functional causes, skeletal correlates, and paleontological implications, Am. J. Phys. Anthropol., 156, 543, 10.1002/ajpa.22699 · DOI
  25. DeSilva, 2018, A nearly complete foot from Dikika, Ethiopia and its implications for the ontogeny and function of Australopithecus afarensis, Sci. Adv., 4, eaar7723, 10.1126/sciadv.aar7723 · DOI
  26. Dingwall, 2013, Hominin stature, body mass, and walking speed estimates based on 1.5 million-year-old fossil footprints at Ileret, Kenya, J. Hum. Evol., 64, 556, 10.1016/j.jhevol.2013.02.004 · DOI
  27. Donelan, 2002, Mechanical work for step-to-step transitions is a major determinant of the metabolic cost of human walking, J. Exp. Biol., 205, 3717, 10.1242/jeb.205.23.3717 · DOI · Paper page
  28. Doran, 1996, Comparative positional behavior of the African apes, 213, 10.1017/CBO9780511752414.018 · DOI
  29. Drapeau, 2013, Metatarsal torsion in monkeys, apes, humans and australopiths, J. Hum. Evol., 64, 93, 10.1016/j.jhevol.2012.10.008 · DOI
  30. Elftman, 1935, Chimpanzee and human feet in bipedal walking, Am. J. Phys. Anthropol., 20, 69, 10.1002/ajpa.1330200109 · DOI
  31. Elftman, 1935, The evolution of the human foot, with especial reference to the joints, J. Anat., 70, 56
  32. Farris, 2012, The mechanics and energetics of human walking and running: a joint level perspective, J. R. Soc. Interface, 9, 110, 10.1098/rsif.2011.0182 · DOI
  33. Fernández, 2016, Form and function of the human and chimpanzee forefoot: implications for early hominin bipedalism, Sci. Rep., 6, 30532, 10.1038/srep30532 · DOI
  34. Fernández, 2018, Evolution and function of the hominin forefoot, Proc. Natl. Acad. Sci. USA, 115, 8746, 10.1073/pnas.1800818115 · DOI
  35. Gefen, 2001, In vivo biomechanical behavior of the human heel pad during the stnce phase of gait, J. Biomech., 34, 1661, 10.1016/S0021-9290(01)00143-9 · DOI
  36. Gill, 2015, Skeletal development of hallucal tarsometatarsal joint curvature and angulation in extant apes and modern humans, J. Hum. Evol., 88, 137, 10.1016/j.jhevol.2015.07.003 · DOI
  37. Greiner, 2014, Kinematics of primate midfoot flexibility, Am. J. Phys. Anthropol., 155, 610, 10.1002/ajpa.22617 · DOI
  38. Griffin, 2010, Comparative in vivo forefoot kinematics of Homo sapiens and Pan paniscus, J. Hum. Evol., 59, 608, 10.1016/j.jhevol.2010.07.017 · DOI
  39. Haile-Selassie, 2012, A new hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations, Nature, 483, 565, 10.1038/nature10922 · DOI
  40. Harcourt-Smith, 2004, Fossils, feet and the evolution of bipedal locomotion, J. Anat., 204, 403, 10.1111/j.0021-8782.2004.00296.x · DOI
  41. Harcourt-Smith, 2015, The foot of Homo naledi, Nat. Commun., 6, 8432, 10.1038/ncomms9432 · DOI
  42. Hatala, 2016, Laetoli footprints reveal bipedal gait biomechanics different from those of modern humans and chimpanzees, Proc. R. Soc. B, 283, 20160235, 10.1098/rspb.2016.0235 · DOI
  43. Hatala, 2016, Footprints reveal direct evidence of group behavior and locomotion in Homo erectus, Sci. Rep., 6, 28766, 10.1038/srep28766 · DOI
  44. Hicks, 1954, The mechanics of the foot. II. The plantar aponeurosis, J. Anat., 88, 25
  45. Hildebrand, 2001, Analysis of Vertebrate Structure
  46. Holowka, 2017, Chimpanzee ankle and foot joint kinematics: arboreal versus terrestrial locomotion, Am. J. Phys. Anthropol., 164, 131, 10.1002/ajpa.23262 · DOI
  47. Holowka, 2017, Chimpanzee and human midfoot motion during bipedal walking and the evolution of the longitudinal arch of the foot, J. Hum. Evol., 104, 23, 10.1016/j.jhevol.2016.12.002 · DOI
  48. Jungers, 2009, Descriptions of the lower limb skeleton of Homo floresiensis, J. Hum. Evol., 57, 538, 10.1016/j.jhevol.2008.08.014 · DOI
  49. Jungers, 2009, The foot of Homo floresiensis, Nature, 459, 81, 10.1038/nature07989 · DOI
  50. Kelly, 2014, Intrinsic foot muscles have the capacity to control deformation of the longitudinal arch, J. R. Soc. Interface, 11, 20131188, 10.1098/rsif.2013.1188 · DOI
  51. Kelly, 2015, Active regulation of longitudinal arch compression and recoil during walking and running, J. R. Soc. Interface, 12, 20141076, 10.1098/rsif.2014.1076 · DOI
  52. Ker, 1987, The spring in the arch of the human foot, Nature, 325, 147, 10.1038/325147a0 · DOI
  53. Kraft, 2014, A natural history of human tree climbing, J. Hum. Evol., 71, 105, 10.1016/j.jhevol.2014.02.002 · DOI
  54. Larson, 2009, Descriptions of the upper limb skeleton of Homo floresiensis, J. Hum. Evol., 57, 555, 10.1016/j.jhevol.2008.06.007 · DOI
  55. Latimer, 1989, The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality, Am. J. Phys. Anthropol., 78, 369, 10.1002/ajpa.1330780306 · DOI
  56. Latimer, 1990, Hallucal tarsometatarsal joint in Australopithecus afarensis, Am. J. Phys. Anthropol., 82, 125, 10.1002/ajpa.1330820202 · DOI
  57. Latimer, 1982, Hominid carpal, metacarpal, and phalangeal bones recovered from the Hadar formation: 1974-1977 collections, Am. J. Phys. Anthropol., 57, 701, 10.1002/ajpa.1330570412 · DOI
  58. Lauder, 1995, On the inference of function from structure, 1
  59. Leakey, 1979, Pliocene footprints in the Laetolil Beds at Laetoli, northern Tanzania, Nature, 278, 317, 10.1038/278317a0 · DOI
  60. Lieberman, 2010, Foot strike patterns and collision forces in habitually barefoot versus shod runners, Nature, 463, 531, 10.1038/nature08723 · DOI
  61. Lovejoy, 2009, Combining prehension and propulsion: the foot of Ardipithecus ramidus, Science, 326, 72e1, 10.1126/science.1175832 · DOI
  62. Masao, 2016, New footprints from Laetoli (Tanzania) provide evidence for marked body size variation in early hominins, Elife, 5, e19568, 10.7554/eLife.19568 · DOI
  63. McDonald, 2016, The role of arch compression and metatarsophalangeal joint dynamics in modulating plantar fascia strain in running, PLoS One, 11, e0152602, 10.1371/journal.pone.0152602 · DOI
  64. McHenry, 2006, Hallucial convergence in early hominids, J. Hum. Evol., 50, 534, 10.1016/j.jhevol.2005.12.008 · DOI
  65. McKeon, 2015, The foot core system: a new paradigm for understanding intrinsic foot muscle function, Br. J. Sports Med., 49, 290, 10.1136/bjsports-2013-092690 · DOI
  66. Moorjani, 2016, Variation in the molecular clock of primates, Proc. Natl. Acad. Sci., 113, 10607, 10.1073/pnas.1600374113 · DOI
  67. Morton, 1922, Evolution of the human foot I, Am. J. Phys. Anthropol., 5, 305, 10.1002/ajpa.1330050409 · DOI
  68. Morton, 1924, Evolution of the human foot II, Am. J. Phys. Anthropol., 7, 1, 10.1002/ajpa.1330070114 · DOI
  69. O'Neill, 2015, Three-dimensional kinematics of the pelvis and hind limbs in chimpanzee (Pan troglodytes) and human bipedal walking, J. Hum. Evol., 86, 32, 10.1016/j.jhevol.2015.05.012 · DOI
  70. Oishi, 2018, Multivariate analysis of variations in intrinsic foot musculature among hominoids, J. Anat., 232, 812, 10.1111/joa.12780 · DOI
  71. Pain, 2001, The role of the heel pad and shank soft tissue during impacts: a further resolution of a paradox, J. Biomech., 34, 327, 10.1016/S0021-9290(00)00199-8 · DOI
  72. Perl, 2012, Effects of footwear and strike type on running economy, Med. Sci. Sports Exerc., 44, 1335, 10.1249/MSS.0b013e318247989e · DOI
  73. Pilbeam, 2017, Reconstructing the last common ancestor of chimpanzees and humans, 22
  74. Pontzer, 2010, Locomotor anatomy and biomechanics of the Dmanisi hominins, J. Hum. Evol., 58, 492, 10.1016/j.jhevol.2010.03.006 · DOI
  75. Pontzer, 2014, Bipedal and quadrupedal locomotion in chimpanzees, J. Hum. Evol., 66, 64, 10.1016/j.jhevol.2013.10.002 · DOI
  76. Prang, 2015, Calcaneal robusticity in Plio-Pleistocene hominins: implications for locomotor diversity and phylogeny, J. Hum. Evol., 80, 135, 10.1016/j.jhevol.2014.09.001 · DOI
  77. Prang, 2015, Rearfoot posture of Australopithecus sediba and the evolution of the hominin longitudinal arch, Sci. Rep., 5, 17677, 10.1038/srep17677 · DOI
  78. Proctor, 2010, Brief Communication: shape analysis of the MT 1 proximal articular surface in fossil hominins and shod and unshod Homo, Am. J. Phys. Anthropol., 143, 631, 10.1002/ajpa.21404 · DOI
  79. Raichlen, 2017, Interpretation of footprints from Site S confirms human-like bipedal biomechanics in Laetoli hominins, J. Hum. Evol., 107, 134, 10.1016/j.jhevol.2017.04.002 · DOI
  80. Raven, 1936, Comparative anatomy of the sole of the foot, Am. Museum Novit., 871, 1
  81. Reeser, 1983, Electromyographic studies of the human foot: experimental approaches to hominid evolution, Foot Ankle, 3, 391, 10.1177/107110078300300607 · DOI
  82. Richmond, 2007, Biomechanics of phalangeal curvature, J. Hum. Evol., 53, 678, 10.1016/j.jhevol.2007.05.011 · DOI
  83. Roberts, 2016, Contribution of elastic tissues to the mechanics and energetics of muscle function during movement, J. Exp. Biol., 219, 266, 10.1242/jeb.124446 · DOI
  84. Rolian, 2009, Walking, running and the evolution of short toes in humans, J. Exp. Biol., 212, 713, 10.1242/jeb.019885 · DOI
  85. Schmitt, 1995, Heel contact as a function of substrate type and speed in primates, Am. J. Phys. Anthropol., 96, 39, 10.1002/ajpa.1330960105 · DOI
  86. Schultz, 1963, Relations between the lengths of the main parts of the foot skeleton in primates, Folia Primatol., 1, 150, 10.1159/000165791 · DOI
  87. Stearne, 2016, The foot's arch and the energetics of human locomotion, Sci. Rep., 6, 19403, 10.1038/srep19403 · DOI
  88. Susman, 1982, Functional morphology of Homo habilis, Science, 217, 931, 10.1126/science.217.4563.931 · DOI
  89. Susman, 1984, Arboreality and bipedality in the Hadar hominids, Folia Primatol. (Basel)., 43, 113, 10.1159/000156176 · DOI
  90. Takahashi, 2017, Energy neutral: the human foot and ankle subsections combine to produce near zero net mechanical work during walking, Sci. Rep., 7, 15404, 10.1038/s41598-017-15218-7 · DOI
  91. Trinkaus, 1996, Neandertal pedal proximal phalanges: diaphyseal loading patterns, J. Hum. Evol., 30, 399, 10.1006/jhev.1996.0035 · DOI
  92. Usherwood, 2012, The human foot and heel–sole–toe walking strategy: a mechanism enabling an inverted pendular gait with low isometric muscle force?, J. R. Soc. Interface, 9, 2396, 10.1098/rsif.2012.0179 · DOI
  93. Venkadesan, 2017, Stiffness of the human foot and evolution of the transverse arch, arXiv
  94. Venkataraman, 2013, Tree climbing and human evolution, Proc. Natl. Acad. Sci. USA, 110, 1237, 10.1073/pnas.1208717110 · DOI
  95. Vereecke, 2008, The mechanics of the gibbon foot and its potential for elastic energy storage during bipedalism, J. Exp. Biol., 211, 3661, 10.1242/jeb.018754 · DOI
  96. Vereecke, 2003, Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus), Am. J. Phys. Anthropol., 120, 373, 10.1002/ajpa.10163 · DOI
  97. Wager, 2016, Elastic energy within the human plantar aponeurosis contributes to arch shortening during the push-off phase of running, J. Biomech., 49, 704, 10.1016/j.jbiomech.2016.02.023 · DOI
  98. Ward, 2011, Complete fourth metatarsal and arches in the foot of Australopithecus afarensis, Science, 331, 750, 10.1126/science.1201463 · DOI
  99. Webber, 2016, The role of plantigrady and heel-strike in the mechanics and energetics of human walking with implications for the evolution of the human foot, J. Exp. Biol., 219, 3729, 10.1242/jeb.138610 · DOI · Paper page
  100. Whittle, 1999, Generation and attenuation of transient impulsive forces beneath the foot: a review, Gait Posture, 10, 264, 10.1016/S0966-6362(99)00041-7 · DOI
  101. Wunderlich, 2017, Foot use during vertical climbing in chimpanzees (Pan troglodytes), J. Hum. Evol., 109, 1, 10.1016/j.jhevol.2017.04.006 · DOI
  102. Yawar, 2017, Contribution of the transverse arch to foot stiffness in humans
  103. Zelik, 2016, A unified perspective on ankle push-off in human walking, J. Exp. Biol., 219, 3676, 10.1242/jeb.140376 · DOI
  104. Zelik, 2018, Ankle and foot power in gait analysis: implications for science, technology and clinical assessment, J. Biomech, 75, 1, 10.1016/j.jbiomech.2018.04.017 · DOI
  105. Zelik, 2015, Six degree-of-freedom analysis of hip, knee, ankle and foot provides updated understanding of biomechanical work during human walking, J. Exp. Biol., 218, 876, 10.1242/jeb.115451 · DOI
  106. Zipfel, 2011, The foot and ankle of Australopithecus sediba, Science, 333, 1417, 10.1126/science.1202703 · DOI

Cited by

Sorted by citations

Metadata

Authors
Holowka, N. B., & Lieberman, D. E.
Affiliations
Department of Human Evolutionary Biology, Harvard University, 11 Divinity Ave, Cambridge, MA 02138, USA
ORCID
Venue
Journal of Experimental Biology
Publisher
The Company of Biologists
Published
2018-09-01
Volume
221
Issue
17
ISSN
  • 1477-9145
  • 0022-0949
DOI
10.1242/jeb.174425
Cited by
135
References
4
Language
en
Licence
www.biologists.com/user-licence-1-1 (vor, 181 d)
Funders
  • Leakey Foundation
  • Wenner-Gren Foundation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review