Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Human Locomotion and Heat Loss: An Evolutionary Perspective

Daniel E. Lieberman

10.1002/cphy.c140011

Source: Volume 5, Issue 1, January 2015

Published online: December 2014

Full Article on Wiley Online Library



Abstract

Humans are unique in many respects including being furless, striding bipeds that excel at walking and running long distances in hot conditions. This review summarizes what we do and do not know about the evolution of these characteristics, and how they are related. Although many details remain poorly known, the first hominins (species more closely related to humans than to chimpanzees) apparently diverged from the chimpanzee lineage because of selection for bipedal walking, probably because it improved their ability to forage efficiently. However, because bipedal hominins are necessarily slow runners, early hominins in open habitats likely benefited from improved abilities to dump heat in order to forage safely during times of peak heat when predators were unable to hunt them. Endurance running capabilities evolved later, probably as adaptations for scavenging and then hunting. If so, then there would have been strong selection for heat‐loss mechanisms, especially sweating, to persistence hunt, in which hunters combine endurance running and tracking to drive their prey into hyperthermia. As modern humans dispersed into a wide range of habitats over the last few hundred thousand years, recent selection has helped populations cope better with a broader range of locomotor and thermoregulatory challenges, but all humans remain essentially adapted for long distance locomotion rather than speed, and to dump rather than retain heat. © 2015 American Physiological Society. Compr Physiol 5:99‐117, 2015.

Comprehensive Physiology offers downloadable PowerPoint presentations of figures for non-profit, educational use, provided the content is not modified and full credit is given to the author and publication.

Download a PowerPoint presentation of all images


Figure 1. Figure 1. Evolutionary tree showing the relationships among humans, chimpanzees, and gorillas, as well as the Last Common Ancestors (LCA) of humans and chimps, and of humans, chimps, and gorillas. The dates of the divergences are only approximate.
Figure 2. Figure 2. Record of the temperature of the earth's oceans based on δ18O from benthic carbonates. Note the general cooling trend over the last 5 million years, but with much variation.
Figure 3. Figure 3. Dates of species of hominins with representative skeletons from each of the major stages of human evolution. Species in the genus Homo are in black, species in the genus Australopithecus are in white, and early hominin species and genera are in gray.
Figure 4. Figure 4. Comparison of major locomotor features in chimpanzees, australopiths, and humans. Highlighted are ancestral features for arboreal locomotion in chimpanzees, derived features for walking in Australopithecus, and derived features for running in Homo.
Figure 5. Figure 5. Schematic of differences between eccrine and apocrine glands (see text for details)
Figure 6. Figure 6. Schematic of differences between vellus and terminal hair (see text for details).
Figure 7. Figure 7. Midsagittal comparison of the external and internal nasal cavities in humans and chimpanzees. Note the lack of a rostrum in humans, combined with the presence of an external nasal cavity, which alters the orientation of flow through the nostrils, producing more turbulent flow.
Figure 8. Figure 8. Scaling of surface area of the turbinates (top) and trachea (bottom) relative to body mass in a wide range of mammals. Humans fall significantly below the line (Data courtesy of T Owerkowicz, summarized in Ref. 88).
Figure 9. Figure 9. Comparison of the face in four hominin species showing variation in the nasal sills and margins. Top left, Australopithecus africanus; Top right, Homo habilis; Bottom left, early African Homo erectus; Bottom right, Homo heidelbergensis. In all species of Homo, the lateral margin of the nasal aperture is everted, indicating the presence of an external nose.
Figure 10. Figure 10. Schematic of Bergmann and Allen's rules, comparing cold‐ versus hot‐adapted body forms (modified, with permission, from Ref. 135). The cold‐adapted body form has a much lower ratio of surface area to volume.


Figure 1. Evolutionary tree showing the relationships among humans, chimpanzees, and gorillas, as well as the Last Common Ancestors (LCA) of humans and chimps, and of humans, chimps, and gorillas. The dates of the divergences are only approximate.


Figure 2. Record of the temperature of the earth's oceans based on δ18O from benthic carbonates. Note the general cooling trend over the last 5 million years, but with much variation.


Figure 3. Dates of species of hominins with representative skeletons from each of the major stages of human evolution. Species in the genus Homo are in black, species in the genus Australopithecus are in white, and early hominin species and genera are in gray.


Figure 4. Comparison of major locomotor features in chimpanzees, australopiths, and humans. Highlighted are ancestral features for arboreal locomotion in chimpanzees, derived features for walking in Australopithecus, and derived features for running in Homo.


Figure 5. Schematic of differences between eccrine and apocrine glands (see text for details)


Figure 6. Schematic of differences between vellus and terminal hair (see text for details).


Figure 7. Midsagittal comparison of the external and internal nasal cavities in humans and chimpanzees. Note the lack of a rostrum in humans, combined with the presence of an external nasal cavity, which alters the orientation of flow through the nostrils, producing more turbulent flow.


Figure 8. Scaling of surface area of the turbinates (top) and trachea (bottom) relative to body mass in a wide range of mammals. Humans fall significantly below the line (Data courtesy of T Owerkowicz, summarized in Ref. 88).


Figure 9. Comparison of the face in four hominin species showing variation in the nasal sills and margins. Top left, Australopithecus africanus; Top right, Homo habilis; Bottom left, early African Homo erectus; Bottom right, Homo heidelbergensis. In all species of Homo, the lateral margin of the nasal aperture is everted, indicating the presence of an external nose.


Figure 10. Schematic of Bergmann and Allen's rules, comparing cold‐ versus hot‐adapted body forms (modified, with permission, from Ref. 135). The cold‐adapted body form has a much lower ratio of surface area to volume.
References
 1. Adelman S , Taylor CR , Heglund MC . Sweating on paws and palms: What is its function. Am J Physiol 229: 1400‐1402, 1975.
 2. Aiello L , Dean MA . An Introduction to Human Evolutionary Anatomy. London: Academic Press, 1990.
 3. Al‐Ramamneh D , Gerken M , Riek A . Effect of shearing on water turnover and thermobiological variables in German Blackhead mutton sheep. J Anim Sci. 89: 4294‐4304, 2011.
 4. Almécija S , Tallman M , Alba DM , Pina M , Moyà‐Solà S , Jungers WL . The femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins. Nat Commun 4: 2888, 2013.
 5. Baccaredda‐Boy A . A note on the cutaneous arterial vessels of some primates. Angiologica 1: 209‐212, 1964.
 6. Barak MM , Lieberman DE , Raichlen D , Pontzer H , Warrener AG , Hublin JJ . Trabecular Evidence for a human‐like gait in Australopithecus africanus . PLoS One 8: e77687, 2013.
 7. Barbujani G , Magagni A , Minch E , Cavalli‐Sforza LL . An apportionment of human DNA diversity. Proc Natl Acad Sci U S A 94: 4516‐4519, 1997.
 8. Bennett MR , Harris JW , Richmond BG , Braun DR , Mbua E , Kiura P , Olago D , Kibunjia M , Omuombo C , Behrensmeyer AK , Huddart D , Gonzalez S . Early hominin foot morphology based on 1.5‐million‐year‐old footprints from Ileret, Kenya. Science. 323: 1197‐1201, 2009.
 9. Berge C , Penin X . Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis. Am J Phys Anthropol 124: 124‐138, 2004.
 10. Biewener AA . Scaling body support in mammals: Limb posture and muscle mechanics. Science. 245: 45‐48, 1989.
 11. Bobe R. Fossil mammals and paleoenvironments in the Omo‐Turkana Basin. Evol Anthropol 20: 254‐263, 2011.
 12. Bolognia JL , Jorizzo J , Schaffer J Dermatology (3rd ed). Philadelphia: WL Saunders, 2012.
 13. Borut A , Dmi'el R , Shkolnik A . Heat balance of resting and walking goats: Comparison of climatic chamber and exposure in the desert. Physiol Zool 52: 105‐112, 1979.
 14. Bramble DM , Jenkins FA Jr . Mammalian locomotor‐respiratory integration: Implications for diaphragmatic and pulmonary design. Science 262: 235‐240. 1993.
 15. Bramble, DM , Lieberman DE. Endurance running and the evolution of Homo . Nature 432: 354‐352, 2004.
 16. Braun DR , Harris JW , Levin NE , McCoy JT , Herries AI , Bamford MK , Bishop LC , Richmond BG , Kibunjia M . Early hominin diet included diverse terrestrial and aquatic animals 1.95 Myr ago in East Turkana, Kenya. Proc Nat Acad Sci USA 107: 10002‐10007, 2010.
 17. Brunet M , Guy F , Pilbeam D , Lieberman DE , Likius A , Mackaye HT , Ponce de León MS , Zollikofer CP , Vignaud P . New material of the earliest hominid from the Upper Miocene of Chad. Nature 434: 752‐755, 2005.
 18. Brunet M , Guy F , Pilbeam D , Mackaye HT , Likius A , Ahounta D , Beauvilain A , Blondel C , Bocherens H , Boisserie JR , De Bonis L , Coppens Y , Dejax J , Denys C , Duringer P , Eisenmann V , Fanone G , Fronty P , Geraads D , Lehmann T , Lihoreau F , Louchart A , Mahamat A , Merceron G , Mouchelin G , Otero O , Pelaez Campomanes P , Ponce De Leon M , Rage JC , Sapanet M , Schuster M , Sudre J , Tassy P , Valentin X , Vignaud P , Viriot L , Zazzo A , Zollikofer C . A new hominid from the upper Miocene of Chad, central Africa. Nature 418: 145‐151, 2002.
 19. Bullard RW , Dill DB , Yousef MK . Responses of the burro to desert heat stress. J Appl Physiol 29: 159‐166, 1970.
 20. Cabanac M . Selective brain cooling in humans: “fancy” or fact? Fed Am Soc Exp Biol 17: 1143‐1146, 1993.
 21. Cabanac M , Brinnel H . Beards, baldness, and sweat secretion. Eu J Appl Physiol Occup Physiol 58: 39‐46, 1988.
 22. Cabanac M , Caputa M . Natural selective cooling of the human brain: Evidence of its occurrence and magnitude. J Physiol 286: 255‐264, 1979.
 23. Carey JW , Steegman, AT Jr . Human nasal protrusion, latitude and climate. Am J Phys Anthropol 56: 313‐319, 1981.
 24. Carrier D . Energetic paradox of human running and hominid evolution. Curr Anthropol 25: 483‐495, 1984.
 25. Cerling TE , Levin NE , Quade J , Wynn JG , Fox DL , Kingston JD , Klein RG , Brown FH . Comment on the paleoenvironment of Ardipithecus ramidus. Science 328: 1105‐1106, 2010.
 26. Cerling TE , Wynn JG , Andanje SA , Bird MI , Korir DK , Levin NE , Mace W , Macharia AN , Quade J , Remien CH . Woody cover and hominin environments in the past 6 million years. Nature 476: 51‐56, 2011.
 27. Churchill SE . Weapon technology, prey size selection and hunting methods in modern hunter‐gatherers: Implications for hunting in the Palaeolithic and Mesolithic. Arch Papers Am Anthropol Assoc 4: 11‐24, 1993.
 28. Churchill SE , Holliday TW , Carlson KJ , Jashashvili T , Macias ME , Mathews S , Sparling TL , Schmid P , de Ruiter DJ , Berger LR . The upper limb of Australopithecus sediba. Science 340: 1233477, 2013.
 29. Churchill SE , Shackelford LL , Georgi JN , Black MT . Morphological variation and airflow dynamics in the human nose. Am J Hum Biol 16: 625‐638, 2004.
 30. Cole P . Modification of inspired air. In: Proctor DF , Andersen HP , editors. The Nose: Upper Airway Physiology and the Atmospheric Environment. Amsterdam: Eslevier Biomedical Press, 1982, pp. 351‐375.
 31. Courtiss EH , Gargan TJ , Courtiss GB . Nasal physiology. Ann Plast Surg 13: 214‐223, 1984.
 32. Crompton RH , Li Y , Thorpe SK , Wang WJ , Savage R , Payne R , Carey TC , Aerts P , Van Elsacker L , Hofstetter A , Gunther MM , D'Aout K , De Clerq D . The biomechanical evolution of erect bipedality. Cour Forsch Inst Senckenberg 243: 115‐126, 2003.
 33. Crompton RH , Vereecke EE , Thorpe SK . 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: 501‐543, 2008.
 34. Daniel PM , Dawes JDK , Pritchard MML . Studies of the carotid rete and its associated arteries. Phil Trans R Soc Lond B 237: 173‐208, 1953.
 35. Darwin CR. The Descent of Man, and Selection in Relation to Sex. London: John Murray, 1871.
 36. Dawson TJ , Blaney CE , Munn AJ , Krockenberger A , Maloney SK . Thermoregulation by kangaroos from mesic and arid habitats: Influence of temperature on routes of heat loss in eastern grey kangaroos (Macropus giganteus) and red kangaroos (Macropus rufus). Physiol Biochem Zool. 73: 374‐381, 2000.
 37. Dawson TJ , Robertshaw D , Taylor CR . Sweating in the kangaroo: A cooling mechanism during exercise, but not in the heat. Am J Physiol 227: 494‐498, 1974.
 38. deMenocal PB . Climate and human evolution. Science 331: 540‐542, 2011.
 39. DeSilva JM , Holt KG , Churchill SE , Carlson KJ , Walker CS , Zipfel B , Berger LR . The lower limb and mechanics of walking in Australopithecus sediba . Science 340: 1232999, 2013.
 40. Dill DB , Edwards HT , Talbott JH . Studies in muscular activity: VII. Factors limiting the capacity for work. J Physiol 77: 49‐62, 1932.
 41. Dingwall HL , Hatala KG , Wunderlich RE , Richmond BG . Hominin stature, body mass, and walking speed estimates based on 1.5 million‐year‐old fossil footprints at Ileret, Kenya. J Hum Evol 64: 556‐568, 2013.
 42. Dominguez‐Rodrigo M . Hunting and scavenging by early humans: The state of the debate. J World Prehist 16: 1‐54, 2002.
 43. Ellis RA , Montagna W . The skin of primates VI. The skin of the gorilla (Gorilla gorilla). Am J Phys Anthropol 20: 79‐85, 1962.
 44. Falk D. Braindance (2nd ed). Gainesville: University Press of Florida, 2004.
 45. Falk D . Constraints on brain size: The radiator hypothesis. In: Kaas JH , Preuss TM , editors. The Evolution of Primate Nervous Systems. Oxford: Elsevier Press, 2007, pp. 347‐354.
 46. Fleagle, JG. Primate Adaptation and Evolution (3rd ed). San Diego: Academic Press, 2013.
 47. Folk GE Jr . Textbook of Environmental Physiology (2nd ed). Philadelphia: Lea and Febiger, 1974.
 48. Folk GE Jr , Semken HA Jr . The evolution of sweat glands. Int J Biometereology 35: 181‐186, 1991.
 49. Foster F , Collard M . A reassessment of Bergmann's rule in modern humans. PLoS One 8: e72269, 2013.
 50. Franciscus RG , Long JC . Variation in human nasal height and breadth. Am J Phys Anthropol 85: 419‐427, 1991.
 51. Franciscus RG , Trinkaus E . Nasal morphology and the emergence of Homo erectus . Am J Phys Anthropol 75: 517‐527, 1988.
 52. Garland T Jr . The relation between maximal running speed and body‐mass in terrestrial mammals. J Zool 199, 157‐170, 1983.
 53. Gisolfi CV , Sato K , Wall PT , Sato F . In vivo and in vitro characteristics of eccrine sweating in patas and rhesus monkeys. J Appl Physiol Respir Environ Exerc Physiol 53: 425‐431, 1982.
 54. Groves CP. A Theory of Human and Primate Evolution. Oxford: Oxford University Press, 1989.
 55. Guy F , Lieberman DE , Pilbeam D , Ponce de Leon M , Likius A , Mackaye HT , Vignaud P , Zollikofer CP , Brunet M . Morphological affinities of the Sahelanthropus tchadensis (Late Miocene hominid from Chad) cranium. Proc Natl Acad Sci USA 102: 18836‐18841, 2005.
 56. Hahn I , Scherer PW , Mozell MM . Velocity profiles measured for airflow through a large‐scale model of the human nasal cavity. J Appl Physiol 75: 2273‐2287, 1993.
 57. Haile‐Selassie Y , Saylor BZ , Deino A , Levin NE , Alene M , Latimer BM . A new hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations. Nature 483: 565‐569, 2012.
 58. Haile‐Selassie Y , Suwa G , White TD . Hominidae. In: Haile‐Selassie Y , WoldeGabriel G , editors. Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia. Berkeley: University of California Press, 2009, pp. 159‐236.
 59. Harcourt‐Smith W , Aiello LC . Fossils, feet and the evolution of human bipedal locomotion. J Anat 204: 403‐416, 2004.
 60. Harcourt‐Smith W . The origins of bipedal locomotion. In: Henke W , Tattersall I , editors. Handbook of Paleoanthropology. Berlin: Springer, 2007, pp. 1483‐1518.
 61. Harrison RJ , Montagna W . Man. New York: Appleton‐Century‐Crofts, 1969.
 62. Hawks J , Wang ET , Cochran GM , Harpending HC , Moyzis RK . Recent acceleration of human adaptive evolution. Proc Natl Acad Sci U S A 104: 20753‐20758, 2007.
 63. Heglund NC , Taylor CR . Speed, stride frequency and energy cost per stride. How do they change with body size and gait? J Exp Biol 138, 301‐318, 1988.
 64. Hewes G . Food transport and the origin of Hominid bipedalism. Am Anthropol 63: 687‐710, 1961.
 65. Hiley PG . The thermoregulatory responses of the galago (Galago crassicaudatus), the baboon (Papio cynocephalus) and the chimpanzee (Pan stayrus) to heat stress. J Physiol 254: 657‐671, 1976.
 66. Holliday TW . Body proportions in Late Pleistocene Europe and modern human origins. J Hum Evol 32: 423‐448, 1997.
 67. Holton NE , Yokley TR , Butaric LN . The morphological interaction between the nasal cavity and maxillary sinuses in living humans. Anat Rec 296: 414‐426, 2013.
 68. Hunt KD . The evolution of human bipedality: Ecology and functional morphology. J Hum Evol 26: 183‐203, 1994.
 69. Jablonski NG , Chaplin G . Epidermal pigmentation in the human lineage is an adaptation to ultraviolet radiation. J Hum Evol 65: 671‐675, 2013.
 70. Jenkinson DM , Robertshaw D . (Studies on the nature of sweat gland ‘fatigue’ in the goat. J Physiol 212: 455‐465, 1971.
 71. Johnson GS , Elizondo RS . Thermoregulation in Macaca mulatta: A thermal balance study. J Appl Physiol 46: 268‐277, 1979.
 72. Jungers WL . Relative joint size and hominid locomotor adaptations with implications for the evolution of hominid bipedalism. J Hum Evol 17: 247‐265, 1988.
 73. Kamberov YG , Wang S , Tan J , Gerbault P , Wark A , Tan L , Yang Y , Li S , Tang K , Chen H , Powell A , Itan Y , Fuller D , Lohmueller J , Mao J , Schachar A , Paymer M , Hostetter E , Byrne E , Burnett M , McMahon AP , Thomas MG , Lieberman DE , Jin L , Tabin CJ , Morgan BA , Sabeti PC . Modeling Recent Human Evolution in Mice by Expression of a Selected EDAR Variant. Cell 152: 691‐702, 2013.
 74. Kelly RL. The Foraging Spectrum: Diversity in Hunter‐Gatherer Lifeways. Clinton Corners, New York: Percheron Press, 2007.
 75. Kimbel WH , White TD , Johanson DC . Cranial morphology of Australopithecus afarensis: A comparative study based on a composite reconstruction. Am J Phys Anthropol 64: 337‐388, 1984.
 76. Kingston JD . Shifting Adaptive Landscapes: Progress and challenges in reconstructing early hominid environments. Yrbk Phys Anthropol 50: 20‐58, 2007.
 77. Kivell TL , Schmitt D . 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, 2009.
 78. Klein RG. The Human Career: Human Biological and Cultural Origins (3rd ed). Chicago: University of Chicago Press, 2009.
 79. Knip AS . Ethnic studies on sweat gland counts. In: Weiner, JS , editor. Physiological Variation and Its Genetic Basis. London: Taylor and Francis, 1977, pp. 113‐123.
 80. Kuno Y. Human Perspiration. Springfield, IL: Charles C Thomas, 1956.
 81. Langdon DH . Umbrella hypotheses and parsimony in human evolution: A critique of the Aquatic Ape Hypothesis. J Hum Evol 33: 479‐494, 1997.
 82. Lebatard AE , Bourlès DL , Duringer P , Jolivet M , Braucher R , Carcaillet J , Schuster M , Arnaud N , Monié P , Lihoreau F , Likius A , Mackaye HT , Vignaud P , Brunet M . Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali Mio‐Pliocene early hominids from Chad. Proc Natl Acad Sci U S A 105: 3226‐3231, 2008.
 83. Lee SS , Piazza SJ . Built for speed: Musculoskeletal structure and sprinting ability. J Exp Biol 212: 3700‐3707, 2009.
 84. Lewis OJ. Functional Morphology of the Evolving Hand and Foot. Oxford: Oxford Univ. Press, 1989.
 85. Lewontin RC . The Apportionment of human diversity. Evol Bio 6: 391‐398, 1972.
 86. Liebenberg L. The Art of Tracking: The Origin of Science. Claremont, South Africa: David Philip Publishers, 2001.
 87. Liebenberg L . Persistence hunting by modern hunter‐gatherers. Curr Anthropol 47: 1017‐1026, 2006.
 88. Lieberman DE. The Evolution of the Human Head. Cambridge MA: Harvard University Press, 2011.
 89. Lieberman DE. The Story of the Human Body: Evolution, Health and Disease. New York: Pantheon, 2013.
 90. Lieberman DE , Bramble DM . The evolution of marathon running: Capabilities in humans. Sports Med 37: 288‐290, 2007.
 91. Lieberman DE , Raichlen DA , Pontzer H , Bramble DM , Cutright‐Smith E The human gluteus maximus and its role in running. J Exp Biol 209: 2143‐2155, 2006.
 92. López Herráez D , Bauchet M , Tang K , Theunert C , Pugach I , Li J , Nandineni MR , Gross A , Scholz M , Stoneking M . Genetic variation and recent positive selection in worldwide human populations: Evidence from nearly 1 million SNPs. PLoS One 4: e7888, 2009.
 93. Lovejoy CO . The origin of man. Science 211: 341‐350, 1981.
 94. Lovejoy CO , Heiple KG , Burstein AH . The gait of Australopithecus. Am J Phys Anthropol 38: 757‐779, 1973.
 95. Lovejoy CO , Latimer B , Suwa G , Asfaw B , White TD . Combining prehension and propulsion: The foot of Ardipithecus ramidus . Science 326: 72e1‐72e8, 2009b.
 96. Lovejoy CO , Suwa G , Spurlock L , Asfaw B , White TD . The pelvis and femur of Ardipithecus ramidus: The emergence of upright walking. Science 326: 71e1‐71e6, 2009a.
 97. MacLatchy L , Gebo D , Kityo R , Pilbeam D . Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J Hum Evol 39: 159‐183, 2000.
 98. Mahoney SA . Cost of locomotion and heat balance during rest and running from 0 to 55° in a patas monkey. J Appl Physiol 49: 789‐800, 1980.
 99. Marks JG , Miller J . Lookingbill and Marks' Principles of Dermatology (4th ed). Philadephia: Saunders, 2006.
 100. Marlowe FW. The Hadza: Hunter‐Gatherers of Tanzania. Berkeley: Univ. California Press, 2010.
 101. Martin RD . Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293: 57‐60, 1981.
 102. McGrew WC. Chimpanzee Material Culture: Implications for Human Evolution. Cambridge: Cambridge University Press. 1992.
 103. Meiri S , Dayan,T . On the validity of Bergmann's rule. J Biogeogr 30: 331‐351, 2003.
 104. Montagna W . The skin of nonhuman primates. Am Zool 12: 109‐124, 1972.
 105. Montagna W , Yun JS . The skin of primates XV. The skin of the chimpanzee (Pan satyrus). Am J Phys Anthropol 21: 189‐203, 1963.
 106. Morgan E. The Aquatic Ape: A Theory of Human Evolution. New York: Stein and Day, 1982.
 107. Niinimaa V . Effect of nasal or oral breathing route on upper airway resistance. Acta Oto‐Laryngologica 95: 161‐166, 1983.
 108. O'Connell JF , Hawkes K , Blurton Jones NG . Hadza scavenging: Implications for Plio‐Pleistocene hominid subsistence. Curr Anthropol 29: 356‐363, 1988.
 109. Olson LG , Strohl KP . The response of the nasal airway to exercise. Am Rev Respir Dis 135: 356‐359, 1987.
 110. Pagel M , Bodmer W . A naked ape would have fewer parasites. Proc Roy Soc B: Biol Sci 270: S117‐S119, 2003.
 111. Passey BH , Levin NE , Cerling TE , Brown FH , Eiler JM . High‐temperature environments of human evolution in East Africa based on bond ordering in paleosol carbonates. Proc Natl Acad Sci U S A 107: 11245‐11249, 2010.
 112. Pickering TR , Bunn HT . The endurance running hypothesis and hunting and scavenging in savanna‐woodlands. J Hum Evol 53: 434‐438, 2007.
 113. Pickford M , Senut B . Millennium ancestor, a 6‐million‐year‐old bipedal hominid from Kenya. Comptes rendus de l'Académie des Sciences de Paris, série 2a, 332: 134‐144, 2001.
 114. Pilbeam D , Young N . Hominoid Evolution: Synthesizing Disparate Data. Comptes Rendus Palevol 3: 303‐319, 2004.
 115. Pontzer H . Predicting the energy cost of terrestrial locomotion: A test of the LiMb model in humans and quadrupeds. J Exp Biol 210: 484‐494, 2007.
 116. Pontzer H . Relating ranging ecology, limb length, and locomotor economy in terrestrial animals. J Theor Biol 296: 6‐12, 2012.
 117. Pontzer H , Raichlen DA , Rodman PS . Bipedal and quadrupedal locomotion in chimpanzees. J Hum Evol 66: 64‐82, 2014.
 118. Pontzer H , Rolian C , Rightmire GP , Jashashvili T , Ponce de León MS , Lordkipanidze D , Zollikofer CP . Locomotor anatomy and biomechanics of the Dmanisi hominins. J Hum Evol 58: 492‐504, 2010.
 119. Pontzer HD , Wrangham RW . The ontogeny of ranging in wild chimpanzees. Int J Primatol 27: 295‐309, 2006.
 120. Raichlen DA , Armstrong H , Lieberman DE . Calcaneus length determines running economy: Implications for endurance running performance in modern humans and Neandertals. J Hum Evol 60: 299‐308, 2011.
 121. Raichlen DA , Gordon AD , Harcourt‐Smith WE , Foster AD , Haas WR . Laetoli footprints preserve earliest direct evidence of human‐like bipedal biomechanics. PLoS One 5: e9769, 2010.
 122. Rantala M . Human nakedness: Adaptation against ectoparasites? Int J Parasitol 29: 1987‐1989, 1999.
 123. Rantala M . Evolution of nakedness in Homo sapiens . J Zool 273: 1‐7, 2007.
 124. Reich D , Patterson N , Kircher M , Delfin F , Nandineni MR , Pugach I , Ko AM , Ko YC , Jinam TA , Phipps ME , Saitou N , Wollstein A , Kayser M , Pääbo S , Stoneking M . Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet 89: 516‐528, 2011.
 125. Richmond BG , Begun DR , Strait DS . Origin of human bipedalism: The knuckle‐walking hypothesis revisited. Yrbk Phys Anthropol 44: 71‐105, 2001.
 126. Richmond BG , Jungers WL . Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319: 1662‐1665, 2008.
 127. Roach NT , Venkadesan M , Rainbow MJ , Lieberman DE . Elastic energy storage in the shoulder and the evolution of high‐speed throwing in Homo . Nature 498: 483‐486, 2013.
 128. Robertshaw D . Sweat and heat exchange in man and other mammals. J Hum Evol 14: 63‐73, 1985.
 129. Robertshaw D . Mechanisms for the control of respiratory evaporative heat loss in panting animals. J Appl Physiol 101: 664‐668, 2006.
 130. Robertshaw D , Taylor CR . A comparison of sweat gland activity in eight species of East African bovids. J Phsyiol 203: 135‐143, 1969.
 131. Rodman PS , McHenry HM . Bioenergetics and the origin of hominid bipedalism. Am J Phys Anthropol 52: 103‐106, 1980.
 132. Rolian C , Lieberman DE , Hamill J , Scott JW , Werbel W . Walking, running and the evolution of short toes in humans. J Exp Biol 212: 713‐721, 2009.
 133. Rubenson J , Heliams DB , Maloney SK , Withers PC , Lloyd DG , Fournier PA . Reappraisal of the comparative cost of human locomotion using gait‐specific allometric analyses. J Exp Biol 210: 3513‐3524, 2007.
 134. Ruff CB. Climatic Adaptation and Hominid Evolution: The Thermoregulatory Imperative. Evol Anthropol 2: 53‐60, 1993.
 135. Ruff CB , Trinkaus E , Walker A , Larsen CS . Postcranial robusticity in Homo, I: Temporal trends and mechanical interpretation. Am J Phys Anthropol 91: 21‐53, 1983.
 136. Ruxton GD , Wilkinson DM . 2011. Avoidance of overheating and selection for both hair loss and bipedality in hominins. Proc Natl Acad Sci U S A 108: 20965‐20969, 2011.
 137. Sabeti PC , Schaffner SF , Fry B , Lohmueller J , Varilly P , Shamovsky O , Palma A , Mikkelsen TS , Altshuler D , Lander ES . Positive natural selection in the human lineage. Science 312: 1614‐1620, 2006.
 138. Saketkhoo K , Kaplan I , Sackner MA . Effect of exercise on nasal mucous velocity and nasal airflow resistance in normal subjects. J Appl Physiol 46: 369‐371, 1979.
 139. Sanders WJ . Comparative morphometric study of the australopithecine vertebral series Stw‐H8/H41. J Hum Evol 34: 249‐302, 1998.
 140. Sankararaman S , Mallick S , Dannemann M , Prüfer K , Kelso J , Pääbo S , Patterson N , Reich D . The genomic landscape of Neanderthal ancestry in present‐day humans. Nature. doi: 10.1038/nature12961, 2014.
 141. Sato F , Owen M , Matthes R , Sato K , Gisolfi CV . Functional and morphological changes in the eccrine sweat gland with heat acclimation. J Appl Physiol 69: 232‐236, 1990.
 142. Sato K , Leidal R , Sato F . Morphology and development of an apoeccrine sweat gland in human axillae. Am J Physiol 252: R166‐R180, 1987.
 143. Scherer PW , Hahn II , Mozell MN . The biophysics of nasal airflow. Otolaryngologic Clin N Am 22: 265‐278, 1989.
 144. Schmidt‐Nielsen K . The physiology of the camel. Scient Am 201: 140‐151, 1959.
 145. Schmidt‐Nielsen K. Desert Animals: Physiological Problems of Heat and Water. Oxford: Clarendon Press, 1964.
 146. Schmidt‐Nielsen K , Bretz WL , Taylor CR . Panting in dogs. Science 169: 1102‐1104, 1970.
 147. Schmitt D . Insights into the evolution of human bipedalism from experimental studies of humans and other primates. J Exp Biol 206: 1437‐1448, 2003.
 148. Schultz AA . The density of hair in primates. Hum Biol 3: 303‐317, 1931.
 149. Schwartz GG , Rosenblum LA . Allometry of primate hair density and the evolution of human hairlessness. Am J Phys Anthropol 55: 9‐12, 1981.
 150. Semaw S , Simpson SW , Quade J , Renne PR , Butler RF , McIntosh WC , Levin N , Dominguez‐Rodrigo M , Rogers MJ . Early Pliocene hominids from Gona, Ethiopia. Nature 433: 301‐305, 2005.
 151. Shea BT . Ontogenetic allometry and scaling: A discussion based on the growth and form of the skull in African apes. In: Jungers WL , editor. Size and Scaling in Primate Morphology. New York: Plenum Press, 1985, pp. 175‐206.
 152. Shea JJ . The origins of lithic projectile point technology: Evidence from Africa, the Levant, and Europe. J Arch Sci 33: 823‐846, 2006.
 153. Shostak M. Nisa, the Life and Words of a !Kung Woman. Cambridge, MA: Harvard University Press, 1981.
 154. Sockol MD , Raichlen D , Pontzer HD . Chimpanzee locomotor energetics and the origin of human bipedalism. Proc Natl Acad Sci U S A 104: 12265‐12269, 2007.
 155. Spoor F , Wood BA , Zonneveld F . Implications of early hominid labyrinthine morphology for the evolution of human bipedal locomotion. Nature 369: 645‐648, 1994.
 156. Steudel‐Numbers KL , Wall‐Scheffler CM . Optimal running speed and the evolution of hominin hunting strategies. J Hum Evol 56: 355‐360, 2009.
 157. Stitt JT, Hardy JD . Thermoregulation in the squirrel monkey (Saimiri sciureus). J Appl Physiol 31: 48‐54, 1971.
 158. Susman RL , Brain TM . New first metatarsal (SKX 5017) from Swartkrans and the gait of Paranthropus robustus . Am J Phys Anthropol 77: 7‐15, 1988.
 159. Susman RL , de Ruiter DJ . New hominin first metatarsal (SK 1813) from Swartkrans. J Hum Evol 47: 171‐181, 2004.
 160. Susman RL , Stern JT Jr , Jungers WL . Arboreality and bipedality in the Hadar hominids. Folia Primatol. 43: 113‐156, 1984.
 161. Taylor CR , Heglund NC , Maloiy GM . Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J Exp Biol 97: 1‐21, 1982.
 162. Taylor CR , Rowntree VJ . Temperature regulation and heat balance in running cheetahs: A strategy for sprinters? Am J Physiol 224: 848‐851, 1973.
 163. Thorpe SKS , Holder RL , Crompton RH . Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316: 1328‐1331, 2007.
 164. Tilkens MJ , Wall‐Scheffler C , Weaver TD , Steudel‐Numbers K . The effects of body proportions on thermoregulation: An experimental assessment of Allen's rule. J Hum Evol 53: 286‐291, 2007.
 165. Trinkaus E . Neanderthal limb proportions and cold adaptations. In: Stringer CB , editor. Aspects of Human Evolution. London: Taylor Francis, 1981, pp. 187‐224.
 166. Turner A . The evolution of the guild of larger terrestrial carnivores during the Plio‐Pleistocene in Africa. Geobios 23: 349‐368, 1990.
 167. Van Valkenburgh B . The dog‐eat‐dog world of carnivores: A review of past and present carnivore community dynamics. In: Stanford CB , Bunn HT , editors. Meat‐Eating and Human Evolution. Oxford: Oxford University Press, 2001, pp. 101‐121.
 168. Vignaud P , Duringer P , Mackaye HT , Likius A , Blondel C , Boisserie JR , De Bonis L , Eisenmann V , Etienne ME , Geraads D , Guy F , Lehmann T , Lihoreau F , Lopez‐Martinez N , Mourer‐Chauviré C , Otero O , Rage JC , Schuster M , Viriot L , Zazzo A , Brunet M . Geology and palaeontology of the Upper Miocene Toros‐Menalla hominid locality, Chad. Nature 418: 152‐155, 2002.
 169. Vogel S. Comparative Biomechanics: Life's Physical Word (2nd ed). Princeton: Princeton University Press, 2013.
 170. Vogt A , McElwee K , Blume‐Peytavi U . Biology of the hair follicle. In: Blume‐Peytavi U , Tosti A , Whiting D , Trüeb R , editors. Hair Growth and Disorders. Berlin: Springer, 2008, pp. 1‐22.
 171. Walker A , Shipman P . The Ape in the Tree: An Intellectual and Natural History of Proconsul. Cambridge, MA: Harvard University Press, 2005.
 172. Ward CV . Interpreting the posture and locomotion of Australopithecus afarensis: Where do we stand? Yrbk Phys Anthropol 35: 185‐215, 2002.
 173. Washburn SL . Tools and human evolution. Sci Am 203: 63‐75, 1960.
 174. Weiner JS . Variation in Sweating. In: Weiner JS , editor. Physiological Variation and Its Genetic Basis. London: Taylor and Francis, 1977, pp. 125‐137.
 175. Wheatley JR , Amis TC , Engel LA . Oronasal partitioning of ventilation during exercise in humans. J Appl Physiol 71: 546‐551, 1991.
 176. Wheeler PE . The evolution of bipedality and loss of functional body hair in hominids. J Hum Evol 13: 91‐98, 1984.
 177. Wheeler PE . The loss of functional body hair in man: The influence of thermal environment, body form and bipedality. J Hum Evol 14: 23‐28, 1985.
 178. Wheeler PE . The thermoregulatory advantages of hominid bipedalism in open equatorial environments: The contribution of increased convective heat loss and cutaneous evaporative cooling. J Hum Evol 21: 107‐115, 1991.
 179. Wheeler PE . The influence of the loss of functional body hair on the water budgets of early hominids. J Hum Evol 23: 379‐ 388, 1992.
 180. White TD , Ambrose SH , Suwa G , Su DF , DeGusta D , Bernor RL , Boisserie JR , Brunet M , Delson E , Frost S , Garcia N , Giaourtsakis IX , Haile‐Selassie Y , Howell FC , Lehmann T , Likius A , Pehlevan C , Saegusa H , Semprebon G , Teaford M , Vrba E . Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus . Science 326: 87‐93, 2009.
 181. White TD , Asfaw B , Beyene Y , Haile‐Selassie Y , Lovejoy CO , Suwa G , WoldeGabriel G . Ardipithecus ramidus and the paleobiology of early hominids. Science 326: 75‐86, 2009.
 182. White TD , Suwa G , Asfaw B . Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371: 306‐312, 1994.
 183. Whittow GC. Comparative Physiology of Thermoregulation. II Mammals. New York: Academic Press, 1971.
 184. Wilkins J , Schoville BJ , Brown KS , Chazan M . Evidence for Early Hafted Hunting Technology. Science 338: 942‐946, 2012.
 185. Wolpoff MH . Climatic influence on the nasal aperture. Am J Phys Anthropol 29: 405‐423, 1968.
 186. Wood B , Harrison T . The evolutionary context of the first hominins. Nature 470: 347‐352, 2012.
 187. Wrangham R , Cheney D , Seyfarth R , Sarmiento E . Shallow‐water habitats as sources of fallback foods for hominins. Am J Phys Anthropol 140: 630‐642, 2009.
 188. Yang N , MacArthur DG , Gulbin JP , Hahn AG , Beggs AH , Easteal S , North K . ACTN3 genotype is associated with human elite athletic performance. Am J Hum Genet 73: 627‐631, 2003.
 189. Yokley TR . Ecogeographic variation in human nasal passages. Am J Phys Anthropol 138: 11‐22, 2009.
 190. Yousef MK , Dill DB . Energy expenditure in desert walks: Man and burro Equus asinus . J Appl Physiol 27: 681‐683, 1969.
 191. Zenker W , Kubik S . Brain cooling in humans – anatomical considerations. Anat Embryol 193: 1‐13, 1996.
 192. Zollikofer CP , Ponce de León MS , Lieberman DE , Guy F , Pilbeam D , Likius A , Mackaye HT , Vignaud P , Brunet M . Virtual cranial reconstruction of Sahelanthropus tchadensis . Nature 434: 755‐759, 2005.

Related Articles:

Adaptation and the Evolution of Physiological Characters
Bioenergetics of Exercising Humans
Integrated Physiological Mechanisms of Exercise Performance, Adaptation, and Maladaptation to Heat Stress
Coping with Thermal Challenges: Physiological Adaptations to Environmental Temperatures

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Human Locomotion and Heat Loss: An Evolutionary Perspective
 

How to Cite

Daniel E. Lieberman. Human Locomotion and Heat Loss: An Evolutionary Perspective. Compr Physiol 2014, 5: 99-117. doi: 10.1002/cphy.c140011