Functional morphology, stable isotopes, and human evolution: A model of consilience

Evolution

Volumn 68, Issue 1, 2014, Pages 190-203

  Yeakel, Justin D ^a   Dominy, Nathaniel J ^b   Koch, Paul L ^a   Mangel, Marc ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Lamont Doherty Earth Observatory   (United States)

^c University of California Santa Cruz   (United States)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

Enamel thickness; Fallback foods; Foraging models; Hominin evolution; Paranthropus; Underground storage organs

Indexed keywords

ABUNDANCE; ENAMEL; EVOLUTIONARY BIOLOGY; FOSSIL RECORD; FUNCTIONAL MORPHOLOGY; HOMINID; ISOTOPIC COMPOSITION; MECHANICAL PROPERTY; PALEONTOLOGY; STABLE ISOTOPE; TOOTH;

PARANTHROPUS; PARANTHROPUS BOISEI; PRIMATES;

CARBON;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; EDIBLE PLANT; ENAMEL; ENAMEL THICKNESS; FALLBACK FOODS; FORAGING MODELS; GENETICS; HISTOLOGY; HOMINID; HOMININ EVOLUTION; HUMAN; MOLAR TOOTH; MOLECULAR EVOLUTION; PARANTHROPUS; PHYSIOLOGY; REPRODUCTIVE FITNESS; UNDERGROUND STORAGE ORGANS;

ENAMEL THICKNESS; FALLBACK FOODS; FORAGING MODELS; HOMININ EVOLUTION; PARANTHROPUS; UNDERGROUND STORAGE ORGANS;

ANIMALS; CARBON ISOTOPES; DENTAL ENAMEL; EVOLUTION, MOLECULAR; GENETIC FITNESS; HOMINIDAE; HUMANS; MODELS, GENETIC; MOLAR; PLANTS, EDIBLE;

EID: 84890873094     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12240     Document Type: Article

References (92)

1. Alberts, S. C., J. A. Hollister-Smith, R. S. Mututua, S. N. Sayialel, P. M. Muruthi, J. K. Warutere, and J. Altmann 2005. Seasonality and long-term change in a savanna environment. Pp. 157-195 in D. K. Brockman and C. P. van Schaik, eds. Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge Univ. Press, Cambridge, U.K.
2. Altmann, S. A. 2009. Fallback foods, eclectic omnivores, and the packaging problem. Am. J. Phys. Anthropol. 140:615-629.
3. Balter, V., J. Braga, P. Télouk, and J. F. Thackeray 2012. Evidence for dietary change but not landscape use in South African early hominins. Nature 489:558-560.
4. 4 grasses under ambient and elevated atmospheric CO 2. Global Change Biol. 10:1565-1575.
5. Barton, R. A., A. Whiten, R. W. Byrne, and M. English 1993. Chemical composition of baboon plant foods: implications for the interpretation of intra- and interspecific differences in diet. Folia Primatol. 61:1-20.
6. Belovsky, G. 1988. An optimal foraging-based model of hunter-gatherer population dynamics. J. Anthropol. Archaeol. 7:329-372.
7. Boccara, N. 2004. Modeling complex systems. Springer, New York.
8. 4 grasses. Oecologia 36:21-32.
9. Boyer, D., G. Ramos-Fernandez, O. Miramontes, J. L. Mateos, G. Cocho, H. Larralde, H. Ramos, and F. Rojas 2006. Scale-free foraging by primates emerges from their interaction with a complex environment. Proc. R. Soc. B 273:1743-1750.
10. Bronikowski, A. M., J. Altmann, D. K. Brockman, M. Cords, L. M. Fedigan, A. Pusey, T. Stoinski, W. F. Morris, K. B. Strier, and S. C. Alberts 2011. Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331:1325-1328.
11. Campbell, A. 1986. The use of wild food plants, and drought in Botswana. J. Arid Environ. 11:81-91.
12. Caswell, H., F. Reed, S. N. Stephenson, and P. Werner 1973. Photosynthetic pathways and selective herbivory: a hypothesis. Am. Nat. 107:465-480.
13. Cerling, T. E., E. Mbua, F. M. Kirera, F. K. Manthi, F. E. Grine, M. G. Leakey, M. Sponheimer, and K. T. Uno 2011. Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proc. Natl. Acad. Sci. USA 108:9337-9341.
14. Clark, C. W., and M. Mangel 2000. Dynamic state variable models in ecology: methods and applications. Oxford Univ. Press, New York.
15. Constantino, P. J. 2013. The "robust" australopiths. Nat. Educ. Knowl. 4:1. Available at http://www.nature.com/scitable/knowledge/library/the-robust-australopiths-84076648.
16. Constantino, P. J., J. J. W. Lee, H. Chai, B. Zipfel, C. Ziscovici, B. R. Lawn, and P. W. Lucas 2010. Tooth chipping can reveal the diet and bite forces of fossil hominins. Biol. Lett. 6:826-829.
17. Copeland, S. 2004. Paleoanthropological implications of vegetation and wild plant resources in modern savanna landscapes, with applications to Plio-Pleistocene Olduvai Gorge, Tanzania. Ph.D. thesis, Rutgers University, New Jersey.
18. Crowley, B. E., and K. E. Samonds 2013. Stable carbon isotope values confirm a recent increase in grasslands in northwestern Madagascar. Holocene 23:1066-1073.
19. Demes, B., and N. Creel 1988. Bite force, diet, and cranial morphology of fossil hominids. J. Hum. Evol. 17:657-670.
20. Dominy, N. J. 2012. Hominins living on the sedge. Proc. Natl. Acad. Sci. USA 109:20171-20172.
21. Dominy, N. J., E. R. Vogel, J. D. Yeakel, P. J. Constantino, and P. W. Lucas 2008. Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evol. Biol. 35:159-175.
22. Dunbar, R. I. M. 1993. Socioecology of the extinct theropiths: a modelling approach. Pp. 465-486 in Theropithecus: the rise and fall of a primate genus. Cambridge Univ. Press, Cambridge, U.K.
23. Galbany, J., J. Altmann, A. Pérez-Pérez, and S. C. Alberts 2011. Age and individual foraging behavior predict tooth wear in Amboseli baboons. Am. J. Phys. Anthropol. 144:51-59.
24. Griffith, C., and B. Long 2010. HOMINIDS: an agent-based spatial simulation model to evaluate behavioral patterns of early Pleistocene hominids. Ecol. Model. 221:738-760.
25. Grine, F. E., M. Sponheimer, P. S. Ungar, J. Lee-Thorp, and M. F. Teaford 2012. Dental microwear and stable isotopes inform the paleoecology of extinct hominins. Am. J. Phys. Anthropol. 148:285-317.
26. Henry, A. G., P. S. Ungar, B. H. Passey, M. Sponheimer, L. Rossouw, M. Bamford, P. Sandberg, D. J. de Ruiter, and L. Berger 2012. The diet of Australopithecus sediba. Nature 487:90-93.
27. Houston, A., and J. M. McNamara 1999. Models of adaptive behaviour. Cambridge Univ. Press, Cambridge, U.K.
28. Janssen, M., J. Sept, and C. Griffith 2007. Hominids foraging in a complex landscape: could Homo ergaster and Australopithecus boisei meet their calories requirements? Pp. 307-318 in Takahashi, S., Sallach, D., and Rouchier, J., eds. Advancing social simulation. Springer Publishing, New York.
29. Jolly, C. J. 1970. The seed-eaters: a new model of hominid differentiation based on a baboon analogy. Man 5:1-26.
30. Juanes, F. 1992. Why do decapod crustaceans prefer small-sized molluscan prey? Mar. Ecol.-Prog. Ser. 87:239-239.
31. Juanes, F., and L. Smith 1995. The ecological consequences of limb damage and loss in decapod crustaceans: a review and prospectus. J. Exp. Mar. Biol. Ecol. 193:197-223.
32. Kay, R. F. 1981. The nut-crackers: a new theory of the adaptations of the Ramapithecinae. Am. J. Phys. Anthropol. 55:141-151.
33. Kay, R. F. 1985. Dental evidence for the diet of Australopithecus. Annu. Rev. Anthropol. 14:315-341.
34. King, S. J., S. J. Arrigo-Nelson, S. T. Pochron, G. M. Semprebon, L. R. Godfrey, P. C. Wright, and J. Jernvall 2005. Dental senescence in a long-lived primate links infant survival to rainfall. Proc. Natl. Acad. Sci. USA 102:16579-16583.
35. Laden, G., and R. Wrangham 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J. Hum. Evol. 49:482-498.
36. Lee-Thorp, J. 2011. The demise of "Nutcracker Man." Proc. Natl. Acad. Sci. USA 108:9319-9320.
37. 4 resources by Pliocene hominins in Chad. Proc. Natl. Acad. Sci. USA 109:20369-20372.
38. Leonard, W., and M. Robertson 1997. Comparative primate energetics and hominid evolution. Am. J. Phys. Anthropol. 102:265-281.
39. Levi, T., F. Lu, D. Yu, and M. Mangel 2011. The behaviour and diet breadth of central-place foragers: an application to human hunters and Neotropical game management. Evol. Ecol. Res. 13:171-185.
40. Lindstedt, S. L., and W. A. Calder III. 1981. Body size, physiological time, and longevity of homeothermic animals. Q. Rev. Biol. 56:1-16.
41. Lucas, P. W. 2004. Dental functional morphology: how teeth work. Cambridge Univ. Press, Cambridge, U.K.
42. Lucas, P. W., I. M. Turner, N. J. Dominy, and N. Yamashita 2000. Mechanical defences to herbivory. Ann. Bot.-Lond. 86:913-920.
43. Lucas, P. W., P. J. Constantino, and B. A. Wood 2008a. Inferences regarding the diet of extinct hominins: structural and functional trends in dental and mandibular morphology within the hominin clade. J. Anat. 212:486-500.
44. Lucas, P. W., P. J. Constantino, B. A. Wood, and B. R. Lawn 2008b. Dental enamel as a dietary indicator in mammals. Bioessays 30:374-385.
45. Lucas, P. W., R. Omar, K. Al-Fadhalah, A. S. Almusallam, A. G. Henry, S. Michael, L. A. Thai, J. Watzke, D. S. Strait, and A. G. Atkins 2012. Mechanisms and causes of wear in tooth enamel: implications for hominin diets. J. R. Soc. Interface 10:20120923.
46. Macho, G. A. 1999. Effects of loading on the biochemical behavior of molars of Homo, Pan, and Pongo. Am. J. Phys. Anthropol. 109:211-227.
47. Mangel, M., and C. W. Clark 1988. Dynamic modeling in behavioral ecology. Princeton Univ. Press, Princeton, NJ.
48. Mangel, M., and D. Ludwig 1992. Definition and evaluation of the fitness of behavioral and developmental programs. Annu. Rev. Ecol. Syst. 23:507-536.
49. Marlowe, F. W. 2003. A critical period for provisioning by Hadza men implications for pair bonding. Evol. Hum. Behav. 24:217-229.
50. Marlowe, F. W., and J. C. Berbesque 2009. Tubers as fallback foods and their impact on Hadza hunter-gatherers. Am. J. Phys. Anthropol. 140:751-758.
51. McArthur, C., and G. D. Sanson 1988. Tooth wear in eastern grey kangaroos (Macropus giganteus) and western grey kangaroos (Macropus fuliginosus), and its potential influence on diet selection, digestion and population parameters. J. Zool. 215:491-504.
52. McGraw, W. S., and D. J. Daegling 2012. Primate feeding and foraging: integrating studies of behavior and morphology. Annu. Rev. Anthropol. 41:203-219.
53. McGraw, W. S., J. D. Pampush, and D. J. Daegling 2012. Enamel thickness and durophagy in mangabeys revisited. Am. J. Phys. Anthropol. 147:326-333.
54. McHenry, H. M. 1988. New estimates of body weights in early hominids and their significance to encephalization and megadontia in "robust" australopithecines. Pp. 133-148 in Evolutionary history of the "Robust" Australopithecines. Transaction Publishers, New Brunswick.
55. Milton, K. 1989. Primate diets and gut morphology: implications for hominid evolution. Pp. 93-116 in Food and evolution: toward a theory of human food habits. Temple Univ. Press, Philadelphia.
56. Organ, C., C. L. Nunn, Z. Machanda, and R. W. Wrangham 2011. Phylogenetic rate shifts in feeding time during the evolution of Homo. Proc. Natl. Acad. Sci. USA 108:14555-14559.
57. Osborne, J. W. 1981. Ageing. Pp. 352-356 in A. H. R. Rowe and R. B. Johns, eds. Dental anatomy and embryology. Vol. 2: A comparison to dental studies. Blackwell, Oxford, U.K.
58. Pate, J. S., and K. W. Dixon 1982. Tuberous, cormous and bulbous plants: biology of an adaptive strategy in Western Australia. University of Western Australia Press, Nedlands, Australia.
59. Perez-Barberia, F. J., and I. J. Gordon 1998. The influence of molar occlusal surface area on the voluntary intake, digestion, chewing behaviour and diet selection of red deer (Cervus elaphus). J. Zool. 245:307-316.
60. Pinder III, J. E., and G. C. Kroh 1987. Insect herbivory and photosynthetic pathways in old-field ecosystems. Ecology 68:254-259.
61. Post, D. G. 1982. Feeding behavior of yellow baboons (Papio cynocephalus) in the Amboseli National Park, Kenya. Int. J. Primatol. 3:403-430.
62. Procheş, Ş., R. M. Cowling, P. Goldblatt, J. C. Manning, and D. A. Snijman 2006. An overview of the Cape geophytes. Biol. J. Linn. Soc. 87:27-43.
63. Rabenold, D., and O. M. Pearson 2011. Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei. PLoS ONE 6:e28379.
64. Raupp, M. J. 1985. Effects of leaf toughness on mandibular wear of the leaf beetle, Plagiodera versicolora. Ecol. Entomol. 10:73-79.
65. Roitberg, B. D., D. R. Gillespie, D. M.J. Quiring, C. R. Alma, W. H. Jenner, J. Perry, J. H. Peterson, M. Salomon, and S. VanLaerhoven 2005. The cost of being an omnivore: mandible wear from plant feeding in a true bug. Naturwissenschaften 92:431-434.
66. Rothman, J. M., D. Raubenheimer, and C. A. Chapman 2011. Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol. Lett. 7:847-849.
67. Sayers, K., M. A. Norconk, and N. L. Conklin-Brittain 2010. Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model. Am. J. Phys. Anthropol. 141:337-357.
68. Schoeninger, M. J., H. T. Bunn, S. S. Murray, and J. A. Marlett 2001. Composition of tubers used by Hadza foragers of Tanzania. J. Food Compos. Anal. 14:15-25.
69. Shellis, R. P., A. D. Beynon, D. J. Reid, and K. M. Hiiemae 1998. Variations in molar enamel thickness among primates. J. Hum. Evol. 35: 507-522.
70. Skogland, T. 1988. Tooth wear by food limitation and its life history consequences in wild reindeer. Oikos 51:238-242.
71. Sponheimer, M., and J. Lee-Thorp 1999. Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283:368.
72. 4 conundrum. Comp. Biochem. Phys. A 136:27-34.
73. Sponheimer, M., J. Lee-Thorp, D. de Ruiter, D. Codron, J. Codron, A. Baugh, and F. Thackeray 2005. Hominins, sedges, and termites: new carbon isotope data from the Sterkfontein valley and Kruger National Park. J. Hum. Evol. 48:301-312.
74. 4 resources? J. Hum. Evol. 51:128-133.
75. Stirling, I. 1969. Tooth wear as a mortality factor in the Weddell seal, Leptonychotes weddelli. J. Mammal. 50:559-565.
76. Swennen, C., L. De Bruijn, P. Duiven, M. Leopold, and E. Marteijn 1983. Differences in bill form of the oystercatcher Haematopus ostralegus; a dynamic adaptation to specific foraging techniques. Neth. J. Sea Res. 17:57-83.
77. Teaford, M. F., and O. J. Oyen 1989. Differences in the rate of molar wear between monkeys raised on different diets. J. Dent. Res. 68:1513-1518.
78. Ungar, P. S., and M. Sponheimer 2011. The diets of early hominins. Science 334:190-193.
79. Ungar, P. S., F. E. Grine, and M. F. Teaford 2008. Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS ONE 3:e2044.
80. Ungar, P. S., R. S. Scott, F. E. Grine, and M. F. Teaford 2010. Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis. Philos. Trans. R. Soc. B 365:3345-3354.
81. Ungar, P. S., K. L. Krueger, R. J. Blumenschine, J. Njau, and R. S. Scott 2012. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. J. Hum. Evol. 63:429-437.
82. Vincent, A. S. 1985. Plant foods in savanna environments: a preliminary report of tubers eaten by the Hadza of Northern Tanzania. World Archaeol. 17:131-148.
83. Vogel, E. R., J. T. van Woerden, P. W. Lucas, S. S. Utami Atmoko, C. P. van Schaik, and N. J. Dominy 2008. Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J. Hum. Evol. 55:60-74.
84. Weishampel, D. B., P. Dodson, and H. Osmólska 2004. The Dinosauria. University of California Press, Berkeley, CA.
85. White, T. D., B. Asfaw, Y. Beyene, Y. Haile-Selassie, C. O. Lovejoy, G. Suwa, and G. Woldegabriel 2009. Ardipithecus ramidus and the paleobiology of early hominids. Science 326:64-64, 75-86.
86. Williams, S. H., B. W. Wright, V. d. Truong, C. R. Daubert, and C. J. Vinyard 2005. Mechanical properties of foods used in experimental studies of primate masticatory function. Am. J. Primatol. 67:329-346.
87. Wolfram Research. 2012. Wolfram|KnowledgeBase. Wolfram Research, Inc., Champaign, Illinois.
88. Wood, B. A., and P. J. Constantino 2007. Paranthropus boisei: fifty years of evidence and analysis. Am. J. Phys. Anthropol. 134:106-132.
89. Wood, B. A., and K. Schroer 2012. Reconstructing the diet of an extinct hominin taxon: the role of extant primate models. Int. J. Primatol. 33:716-742.
90. Yamashita, N., C. J. Vinyard, and C. L. Tan 2009. Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. Am. J. Phys. Anthropol. 139:368-381.
91. Yeakel, J. D., N. C. Bennett, P. L. Koch, and N. J. Dominy 2007. The isotopic ecology of African mole rats informs hypotheses on the evolution of human diet. Proc. R. Soc. B 274:1723-1730.
92. Youngblood, D. 2004. Identifications and quantification of edible plant foods in the Upper (Nama) Karoo, South Africa. Econ. Bot. 58:S43-S65.