Costs of encephalization: the energy trade-off hypothesis tested on birds

Journal of Human Evolution

Volumn 51, Issue 3, 2006, Pages 228-243

  Isler, Karin ^a   van Schaik, Carel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Brain size; Digestion; Expensive Tissue Hypothesis; Gut size; Locomotion; Reproduction

Indexed keywords

BIRD; BRAIN; LOCOMOTION; PHYLOGENETICS; PRIMATE;

AVES; HOMINIDAE; MAMMALIA; PRIMATES;

EID: 33747069140     PISSN: 00472484     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhevol.2006.03.006     Document Type: Article

References (125)

1. Aiello L.C., Bates N., and Joffe T. In defence of the expensive tissue hypothesis. In: Falk D., and Gibson K.R. (Eds). Evolutionary Anatomy of the Primate Cerebral Cortex (2001), Cambridge University Press, Cambridge 57-78
2. Aiello L.C., and Key C. Energetic consequences of being a Homo erectus female. Am. J. Hum. Biol. 14 (2002) 551-565
3. Aiello L.C., and Wells J.C.K. Energetics and the evolution of the genus Homo. Ann. Rev. Anthropol. 31 (2002) 323-338
4. Aiello L.C., and Wheeler P. The expensive-tissue hypothesis - the brain and the digestive-system in human and primate evolution. Curr. Anthropol. 36 (1995) 199-221
5. Alexander R.M. Models and the scaling of energy costs for locomotion. J. Exp. Biol. 208 (2005) 1645-1652
6. Armstrong E. Relative brain size and metabolism in mammals. Science 220 (1983) 1302-1304
7. Barton R.A. The evolutionary ecology of the primate brain. In: Lee P.C. (Ed). Comparative Primate Socioecology (1999), Cambridge University Press, Cambridge 167-194
8. Battley P.F., Piersma T., Dietz M.W., Tang S.X., Dekinga A., and Hulsman K. Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc. R. Soc. Lond. B-Biol. Sci. 267 (2000) 191-195
9. Bennett P.M., and Harvey P.H. Brain size, development and metabolism in birds and mammals. J. Zool. 207 (1985) 491-509
10. Bennett P.M., and Harvey P.H. Relative brain size and ecology in birds. J. Zool. 207 (1985) 151-169
11. Blackburn T.M. An interspecific relationship between egg size and clutch size in birds. Auk 108 (1991) 973-977
12. Bleiweiss R., Kirsch J.A.W., and Matheus J.C. DNA hybridization evidence for the principal lineages of hummingbirds (Aves: Trochilidae). Mol. Biol. Evol. 14 (1997) 325-343
13. Butler P.J. Exercise in birds. J. Exp. Biol. 160 (1991) 233-262
14. Cartmill M. Paleoanthropology: science or mythological charter?. J. Anthropol. Res. 58 (2002) 183-201
15. Caton J.S., Bauer M.L., and Hidari H. Metabolic components of energy expenditure in growing beef cattle - Review. Asian-Australasian. J. Anim. Sci. 13 (2000) 702-710
16. Chivers D.J., and Hladik C.M. Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J. Morphol. 166 (1980) 337-386
17. Cibois A., and Pasquet E. Molecular analysis of the phylogeny of 11 genera of the Corvidae. Ibis 141 (1999) 297-306
18. Cibois A., Pasquet E., and Schulenberg T.S. Molecular systematics of the Malagasy babblers (Passeriformes: Timaliidae) and warblers (Passeriformes: Sylviidae), based on cytochrome b and 16S rRNA sequences. Mol. Phylogenet. Evol. 13 (1999) 581-595
19. Clarys J.P., Martin A.D., Marfell-Jones M.J., Janssens V., Caboor D., and Drinkwater D.T. Human body composition: a review of adult dissection data. Am. J. Hum. Biol. 11 (1999) 167-174
20. Clutton-Brock T.H., and Harvey P.H. Primates, brains and ecology. J. Zool. 190 (1980) 309-323
21. Cohen B.L., Baker A.J., Bleschschmidt K., Dittmann D.L., Furness R.W., Gerwin J.A., Helbig A.J., DeKorte J., Marshall H.D., Palma R.L., Peter H.U., Ramli R., Siebold I., Willcox M.S., Wilson R.H., and Zink R.M. Enigmatic phylogeny of skuas (Aves: Stercorariidae). Proc. R. Soc. Lond. B-Biol. Sci. 264 (1997) 181-190
22. Crile G.W., and Quiring D.P. A record of the body weights and certain organ and gland weights of 3690 animals. Ohio J. Sci. 40 (1940) 219-259
23. Crochet P.-A., Bonhomme F., and Lebretton J.-D. Molecular phylogeny and plumage evolution in gulls (Larini). J. Evol. Biol. 13 (2000) 47-57
24. Daan S., Masman D., and Groenewold A. Avian basal metabolic rates - their association with body composition and energy expenditure in nature. Am. J. Physiol. 259 (1990) R333-R340
25. DeFilippis V.R., and Moore W.S. Resolution of phylogenetic relationships among recently evolved species as a function of amount of DNA sequence: an empirical study based on woodpeckers (Aves: Picidae). Mol. Phylogenet. Evol. 16 (2000) 143-160
26. DeGolier T.F., Mahoney S.A., and Duke G.E. Relationships of avian cecal lengths to food habits, taxonomic position, and intestinal lengths. Condor 101 (1999) 622-634
27. Dimcheff D.E., Drovetski S.V., and Mindell D.P. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol. Phylogenet. Evol. 24 (2002) 203-215
28. Donne-Goussé C., Laudet V., and Hänni C. A molecular phylogeny of anseriformes based on mitochondrial DNA analysis. Mol. Phylogenet. Evol. 23 (2002) 339-356
29. Dunbar R.I.M. Neocortex size as a constraint on group size in primates. J. Hum. Evol. 22 (1992) 469-493
30. Dunbar R.I.M. The social brain hypothesis. Evol. Anthropol. 6 (1998) 178-190
31. Dunbar R.I.M. The social brain: mind, language, and society in evolutionary perspective. Annu. Rev. Anthropol. 32 (2003) 163-181
32. Dunning J. CRC Handbook of Avian Body Masses (1993), CRC Press
33. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 125 (1985) 1-15
34. Fish J.L., and Lockwood C.A. Dietary constraints on encephalization in primates. Am. J. Phys. Anthropol. 120 (2003) 171-181
35. Garland T., Harvey P.H., and Ives A.R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41 (1992) 18-32
36. Greenewalt C.H. Dimensional relationships for flying animals. Smithson. Misc. Collect. 144 no. 2 (1962)
37. Güntert M. Morphologische Untersuchungen zur adaptiven Radiation des Verdauungstraktes bei Papageien (Psittaci). Zool. Jb. Anat. 106 (1981) 471-526
38. Harvey P.H., and Krebs J.R. Comparing brains. Science 249 (1990) 140-146
39. Hofman M.A. Energy metabolism, brain size and longevity in mammals. Q. Rev. Biol. 58 (1983) 495-512
40. In: del Hoyo J., Elliott J., and Sargatal J. (Eds). Handbook of the Birds of the World (1992-2004), Lynx Editions, Barcelona
41. Hume I.D., and Biebach H. Digestive tract function in the long-distance migratory garden warbler, Sylvia borin. J. Comp. Physiol. (B) 166 (1996) 388-395
42. Hutcheon J.M., Kirsch J.W., and Garland T. A comparative analysis of brain size in relation to foraging ecology and phylogeny in the chiroptera. Brain Behav. Evol. 60 (2002) 165-180
43. Irestedt M., Fjeldsa J., Nylander J.A.A., and Ericson P.G.P. Phylogenetic relationships of typical antbirds (Thamnophilidae) and test of incongruence based on Bayes factors. BMC Evol. Biol. 4 art. no. 23 (2004)
44. Isler K., Barbour A.D., and Martin R.D. Line-fitting by rotation: a nonparametric method for bivariate allometric analysis. Biom. J. 44 (2002) 289-304
45. Isler, K., Payne, R.C., Günther, M.M., Thorpe, S.K.S., Li, Y., Savage, R., Crompton, R.H. Inertial properties of hominoid limb segments. J. Anat., in press
46. Iwaniuk A., and Nelson J. A comparative analysis of relative brain size in Waterfowl (Anseriformes). Brain Behav. Evol. 57 (2001) 87-97
47. Iwaniuk A., and Nelson J. Can endocranial volume be used as an estimate of brain size in birds?. Can. J. Zool. 80 (2002) 16-23
48. Iwaniuk A.N., Dean K.M., and Nelson J.E. A mosaic pattern characterizes the evolution of the avian brain. Proc. R. Soc. Lond. B-Biol. Sci. 271 (2004) S148-S151
49. Iwaniuk A.N., and Nelson J.E. Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can. J. Zool. 81 (2003) 1913-1928
50. Jones K.E., and MacLarnon A.M. Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat. 164 (2004) E20-E31
51. Kaufman J.A., Hladik C.M., and Pasquet P. On the expensive-tissue hypothesis: independent support from highly encephalized fish. Curr. Anthropol. 44 (2003) 705-707
52. Kersten M., and Piersma T. High-levels of energy-expenditure in shorebirds - metabolic adaptations to an energetically expensive way of life. Ardea 75 (1987) 175-187
53. Kohler M., and Moya-Sola S. Reduction of brain and sense organs in the fossil insular bovid Myotragus. Brain Behav. Evol. 63 (2004) 125-140
54. Konarzewski M., and Diamond J. Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49 (1995) 1239-1248
55. Koteja P. On the relation between basal and field metabolic rates in birds and mammals. Funct. Ecol. 5 (1991) 56-64
56. Kotrschal K., Van Staaden M.J., and Huber R. Fish brains: evolution and environmental relationships. Rev. Fish Biol. Fish. 8 (1998) 373-408
57. Kramer P.A., and Eck G.G. Locomotor energetics and leg length in hominid bipedality. J. Hum. Evol. 38 (2000) 651-666
58. Landolt R. Vergleichend funktionelle Morphologie des Verdauungstraktes der Tauben (Columbidae) mit besonderer Berücksichtigung der adaptiven Radiation der Fruchttauben (Treroninae). Teil I. Zool. Jb. Anat. 116 (1987) 169-215
59. Landolt R. Vergleichend funktionelle Morphologie des Verdauungstraktes der Tauben (Columbidae) mit besonderer Berücksichtigung der adaptiven Radiation der Fruchttauben (Treroninae). Teil II (Schluss). Zool. Jb. Anat. 116 (1987) 285-316
60. Langer P. Lactation, weaning period, food quality, and digestive tract differentiations in eutheria. Evolution 57 (2003) 1196-1215
61. Lefebvre L., Reader S.M., and Sol D. Brains, innovations and evolution in birds and primates. Brain Behav. Evol. 63 (2004) 233-246
62. Leonard W.R., and Robertson M.L. Evolutionary perspectives on human nutrition - the influence of brain and body size on diet and metabolism. Am. J. Hum. Biol. 6 (1994) 77-88
63. Leonard W.R., and Robertson M.L. Comparative primate energetics and hominid evolution. Am. J. Phys. Anthropol. 102 (1997) 265-281
64. Leonard W.R., Robertson M.L., Snodgrass J.J., and Kuzawa C.W. Metabolic correlates of hominid brain evolution. Comp. Biochem. Physiol. A-Molec. Integr. Physiol. 136 (2003) 5-15
65. Lindstedt S.L., and Schaeffer P.J. Use of allometry in predicting anatomical and physiological parameters of mammals. Lab. Anim. 36 (2002) 1-19
66. Lindstrom A., Kvist A., Piersma T., Dekinga A., and Dietz M.W. Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J. Exp. Biol. 203 (2000) 913-919
67. Livezey B.C. Phylogeny and evolutionary ecology of modern seaducks (Anatidae: Mergini). Condor 97 (1995) 233-255
68. Livezey B.C. A phylogenetic analysis of modern pochards (Anatidae: Aythyini). Auk 113 (1996) 74-93
69. MacLarnon A.M., Chivers D.J., and Martin R.D. Gastro-intestinal allometry in primates and other mammals including new species. In: Else J.G., and Lee P. (Eds). Primate Ecology and Conservation (1986), Cambridge University Press, Cambridge 75-85
70. Magnan A. Les caractéristiques des oiseaux suivant le mode de vol. Ann. Sci. Nat. Zool. Biol. Anim. 10 (1922) 125-334
71. Marden J.H. Maximum lift production during takeoff in flying animals. J. Exp. Biol. 130 (1987) 235-258
72. Marden J.H. Maximum load-lifting and induced power output of Harris hawks are general functions of flight-muscle mass. J. Exp. Biol. 149 (1990) 511-514
73. Marino L. A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain Behav. Evol. 51 (1998) 230-238
74. Martin R.D. Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol. Sci. 11 (1996) 149-156
75. Martin R.D. Comparative aspects of human brain evolution: scaling, energy costs and confounding variables. In: Jablonski N.G., and Aiello L.C. (Eds). The Origin and Diversification of Language (1998), University of California Press, San Francisco 35-68
76. Martin R.D., and Barbour A.D. Aspects of line-fitting in bivariate allometric analyses. Folia Primatol. 53 (1989) 65-81
77. Martin R.D., Genoud M., and Hemelrijk C. Problems of allometric scaling analysis: examples from mammalian reproductive biology. J. Exp. Biol. 208 (2005) 1731-1747
78. McKechnie A.E., and Wolf B.O. The allometry of avian basal metabolic rate: good predictions need good data. Physiol. Biochem. Zool 77 (2004) 502-521
79. McNab B.K. Energy-conservation and the evolution of flightlessness in birds. Am. Nat. 144 (1994) 628-642
80. McNab B.K. The Physiological Ecology of Vertebrates: A View from Energetics (2002), Cornell University Press, Ithaca, New York
81. McNab B.K., and Eisenberg J.F. Brain size and its relation to the rate of metabolism in mammals. Am. Nat. 133 (1989) 157-167
82. Milton K. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am. Anthropol. 83 (1981) 534-548
83. Mink J.W., Blumenschine R.J., and Adams D.B. Ratio of central nervous system to body metabolism in vertebrates - its constancy and functional basis. Am. J. Physiol. 241 (1981) R203-R212
84. Mlikovsky J. Brain size in birds: 1. Tinamiformes through Ciconiiformes. Acta Soc. Zool. Bohemoslov. 53 (1989) 33-47
85. Mlikovsky J. Brain size in birds: 2. Falconiformes through Gaviiformes. Acta Soc. Zool. Bohemoslov. 53 (1989) 200-213
86. Mlikovsky J. Brain size in birds: 3. Columbiformes through Piciformes. Acta Soc. Zool. Bohemoslov. 53 (1989) 252-264
87. Mlikovsky J. Brain size in birds: 4. Passeriformes. Acta Soc. Zool. Bohemoslov. 54 (1990) 27-37
88. Morbeck M.E., and Zihlman A.L. Body composition and limb proportions. In: Schwartz J.H. (Ed). Orang-Utan Biology (1988), Oxford University Press, Oxford 285-297
89. Nealen P.M., and Ricklefs R.E. Early diversification of the avian brain: body relationship. J. Zool. 253 (2001) 391-404
90. Oelhafen M.G. Vergleichend morphologische Untersuchungen am Verdauungstrakt einheimischer Rabenvögel (Corvidae). Ornithol. Beob. 78 (1981) 17-40
91. Pagel M.D., and Harvey P.H. How mammals produce large-brained offspring. Evolution 42 (1988) 948-957
92. Payne, R., 2001. Musculoskeletal Adaptations for Climbing in Hominoids and Their Role as Exaptions for the Acquisition of Bipedalism. Ph.D. thesis, Liverpool University, Liverpool.
93. Payne, R.C., Crompton, R.H., Günther, M.M., D'Août, K., Savage, R., Isler, K., Vereecke, E. Morphological analysis of the hindlimb in apes and humans. Part I: Muscle architecture. J. Anat., in press.
94. Pennycuick C.J. Computer simulation of fat and muscle burn in long-distance bird migration. J. Theor. Biol. 191 (1998) 47-61
95. Piersma T. Energetic bottlenecks and other design constraints in avian annual cycles. Integr. Comp. Biol. 42 (2002) 51-67
96. Piersma T., Bruinzeel L., Drent R., Kersten M., VanderMeer J., and Wiersma P. Variability in basal metabolic rate of a long-distance migrant shorebird (Red Knot, Calidris canutus) reflects shifts in organ sizes. Physiol. Biochem. Zool. 69 (1996) 191-217
97. Piersma T., Gudmundsson G.A., and Lilliendahl K. Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72 (1999) 405-415
98. Pitnick S., Jones K.E., and Wilkinson G.S. Mating systems and brain size in bats. Proc. R. Soc. Lond. B-Biol. Sci. 273 (2006) 719-724
99. Pontzer H., and Wrangham R.W. Climbing and the daily energy cost of locomotion in wild chimpanzees: implications for hominoid locomotor evolution. J. Hum. Evol. 46 (2004) 317-335
100. Portmann A. Etudes sur la cérébralisation chez les oiseaux. I. Alauda 14 (1946) 2-20
101. Portmann A. Etudes sur la cérébralisation chez les oiseaux. III. Cérébralisation et mode ontogenetique. Alauda 15 (1947) 161-171
102. Prothero J.W. Organ scaling in mammals - the liver. Comp. Biochem. Physiol. A-Physiol. 71 (1982) 567-577
103. Prothero J.W. Organ scaling in mammals - the kidneys. Comp. Biochem. Physiol. A-Physiol. 77 (1984) 133-138
104. Rehkamper G., Frahm H.D., and Zilles K. Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (Insectivores and Primates). Brain Behav. Evol. 37 (1991) 125-143
105. Ricklefs R.E., Konarzewski M., and Daan S. The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am. Nat. 147 (1996) 1047-1071
106. Rodman P.S., and McHenry H.M. Bioenergetics and the origin of hominid bipedalism. Am. J. Phys. Anthropol. 52 (1980) 103-106
107. Safi K., Seid M.A., and Dechmann D.K.N. Bigger is not always better: when brains get smaller. Biol. Lett. 1 (2005) 283-285
108. Schönwetter M. Handbuch der Oologie (1960-1978), Akademie Verlag, Berlin
109. Sheldon B.C., and Winkler D.W. Intergeneric phylogenetic relationships of swallows estimated by DNA-DNA hybridization. Auk 110 (1993) 798-824
110. Sheldon F.H., Slikas B., Kinnarney M., Gill F.B., Zhao E., and Silverin B. DNA-DNA hybridization evidence of phylogenetic relationships among major lineages of Parus. Auk 109 (1992) 173-185
111. Sibley C.G., Ahlquist J.E., and Monroe B.L. A classification of the living birds of the world based on DNA-DNA hybridization studies. Auk 105 (1988) 409-423
112. Sibley C.G., and Monroe B.L. Distribution and Taxonomy of Birds of the World (1990), Yale University Press, New Haven and London
113. Sol D., Lefebvre L., and Rodriguez-Teijeiro J.D. Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proc. R. Soc. Lond. B-Biol. Sci. 272 (2005) 1433-1441
114. Speakman J.R., and Selman C. Physical activity and resting metabolic rate. Proc. Nutr. Soc. 62 (2003) 621-634
115. Starck J., and Ricklefs R. Patterns of development: the altricial-precocial spectrum. In: Starck J., and Ricklefs R. (Eds). Avian Growth and Development: Evolution within the Altricial-Precocial Spectrum (1998), Oxford University Press, Oxford 3-30
116. Starck J.M. Structural flexibility of the gastro-intestinal tract of vertebrates - Implications for evolutionary morphology. Zool. Anz. 238 (1999) 87-101
117. Stephan H. Methodische Studien über den quantitativen Vergleich architektonischer Struktureinheiten des Gehirns. Z. Wiss. Zool. 164 (1960) 143-172
118. Stern Jr. J.T. Climbing to the top: a personal memoir of Australopithecus afarensis. Evol. Anthropol. (2000) 113-133
119. Towe A.L., and Mann M.D. Brain size body length relations among myomorph rodents. Brain Behav. Evol. 39 (1992) 17-23
120. Viscor G., and Fuster J.F. Relationships between morphological parameters in birds with different flying habits. Comp. Biochem. Physiol. A-Physiol. 87 (1987) 231-249
121. Yuri T., and Mindell D.P. Molecular phylogenetic analysis of Fringillidae, "New World nine-primaried oscines" (Aves: Passeriformes). Mol. Phylogenet. Evol. 23 (2002) 229-243
122. Zihlman A.L. Body build and tissue composition in Pan paniscus and Pan troglodytes, with comparisons to other hominoids. In: Susman R.L. (Ed). The Pygmy Chimpanzee (1984), Plenum Press, New York 179-200
123. Zihlman A.L., and McFarland R.K. Body mass in lowland gorillas: a quantitative analysis. Am. J. Phys. Anthropol. 113 (2000) 61-78
124. Ziswiler V. Vergleichend morphologische Untersuchungen am Verdauungstrakt körnerfressender Singvögel zur Abklärung ihrer systematischen Stellung. Zool. Jb. Syst. 94 (1967) 427-520
125. Ziswiler, V., Güttinger, H.R., Bregulla, H., 1972. Monographie der Gattung Erythrura Swainson, 1837 (Aves, Passeres, Estrildidae). Zoologisches Forschungsinstitut und Museum Alexander König, Bonn.