Primate brains, the 'island rule' and the evolution of Homo floresiensis

Journal of Human Evolution

Volumn 65, Issue 6, 2013, Pages 750-760

  Montgomery, Stephen H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Allometry; Body mass; Brain size; Dwarfism; Insularity

Indexed keywords

ALLOMETRY; BODY MASS; BODY SIZE; BRAIN; HOMINID; HUMAN EVOLUTION; PHYLOGENETICS; PRIMATE;

HOMO FLORESIENSIS; MAMMALIA; PRIMATES;

ALLOMETRY; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY MASS; BRAIN; BRAIN SIZE; CLASSIFICATION; DWARFISM; EVOLUTION; FOSSIL; GENETICS; HISTOLOGY; HOMINID; INDONESIA; INSULARITY; ISLAND (GEOLOGICAL); PHYLOGENY; PRIMATE;

ALLOMETRY; BODY MASS; BRAIN SIZE; DWARFISM; INSULARITY;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; FOSSILS; HOMINIDAE; INDONESIA; ISLANDS; MODELS, BIOLOGICAL; PHYLOGENY; PRIMATES;

EID: 84887615014     PISSN: 00472484     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhevol.2013.08.006     Document Type: Article

References (90)

1. Aiello L.C. Five years of Homo floresiensis. Am. J. Phys. Anthropol. 2010, 142:167-179.
2. Aiello L.C., Wheeler P. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 1995, 36:199-221.
3. Argue D., Morwood M., Sutikna T., Jatmiko, Saptomo W.E. Homo floresiensis: a cladistic analysis. J.Hum. Evol. 2009, 57:623-639.
4. Arnold C., Matthews L.J., Nunn C.L. The 10k trees website: a new online resource for primate phylogeny. Evol. Anthropol. 2010, 19:114-118.
5. Baab K.L. Homo floresiensis: making sense of the small-bodied hominin fossils from Flores. Nat. Educ. Knowl. 2012, 3:4.
6. Baab K.L., McNulty K.P. Size, shape, and asymmetry in fossil hominins: the status of the LB1 cranium based on 3D morphometric analyses. J.Hum. Evol. 2009, 57:608-622.
7. Berger L.R., de Ruiter D.J., Churchill S.E., Schmid P., Carlson K.J., Dirks P.H.G.M., Kibii J.M. Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 2010, 328:195-204.
8. Bininda-Emonds O.R.P., Cardillo M., Jones K.E., MacPhee R.D.E., Beck R.M.D., Grenyer R., Price S.A., Vos R.A., Gittleman J.L., Purvis A. The delayed rise of present-day mammals. Nature 2007, 446:507-512.
9. Bollen K.A., Jackman R.W. Regression diagnostics: an expository treatment of outliers and influential cases. Modern Methods of Data Analysis 1990, 257-291. Sage, Newbury Park. J. Fox, J.S. Long (Eds.).
10. Bromham L., Cardillo M. Primates follow the 'island rule': implications for interpreting Homo floresiensis. Biol. Lett. 2007, 3:398-400.
11. Brown P. LB1 and LB6 Homo floresiensis are not modern human (Homo sapiens) cretins. J.Hum. Evol. 2012, 62:201-224.
12. Brown P., Maeda T. Liang Bua Homo floresiensis mandibles and mandibular teeth: a contribution to the comparative morphology of a new hominin species. J.Hum. Evol. 2009, 57:571-596.
13. Brown P., Sutikna T., Morwood M.J., Soejono R.P., Jatmiko, Saptomo W.E., Due Rokus Awe Anew small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 2004, 431:1055-1061.
14. Brumm A., Jensen G.M., van den Bergh G.D., Morwood M.J., Kurniawan I., Aziz F., Storey M. Hominins on Flores, Indonesia, by one million years ago. Nature 2010, 464:748-752.
15. Carlson K.J., Stout D., Jashashvili T., de Ruiter D.J., Tafforeau P., Carlson K., Berger L.R. The endocast of MH1, Australopithecus sediba. Science 2011, 333:1402-1407.
16. Chatterjee H.J., Ho S.Y.W., Barnes I., Groves C. Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol. Biol. 2009, 9:259.
17. Cook D.R. Detection of influential observation in linear regression. Technometrics 1977, 19:15-18.
18. Deaner R.O., Isler K., Burkart J., van Schaik C. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 2007, 70:115-124.
19. Dennell R., Roebroeks W. An Asian perspective on early human dispersal from Africa. Nature 2005, 438:1099-1104.
20. Falk D., Hildebolt C., Smith K., Morwood M.J., Sutikna T., Brown P., Jatmiko, Saptomo W.E., Brunsden B., Prior F. The brain of LB1, Homo floresiensis. Science 2005, 308:242-245.
21. Falk D., Hildebolt C., Smith K., Morwood M.J., Sutikna T., Jatmiko, Saptomo E.W., Brunsden B., Prior F. Response to comment on "The brain of LB1 Homo floresiensis". Science 2006, 312:999.
22. Falk D., Hildebolt C., Smith K., Jungers W., Larson S., Morwood M., Sutikna T., Jatmiko, Saptomo E.W., Prior F. The type specimen (LB1) of Homo floresiensis did not have Laron syndrome. Am. J. Phys. Anthropol. 2009, 140:52-63.
23. Falk D., Hildebolt C., Smith K., Morwood M.J., Sutikna T., Jatmiko, Wayhu Saptomo E., Prior F. LB1's virtual endocast, microcephaly, and hominin brain evolution. J.Hum. Evol. 2009, 57:597-607.
24. Ferring R., Oms O., Agusti J., Berna F., Nioradze M., Shelia T., Tappen M., Vekua A., Zhvania D., Lordkipanidze D. Earliest human occupations at Dmanisi (Georgian Caucasus) dated to 1.85-1.78Ma. Proc. Natl. Acad. Sci. 2011, 108:10432-10436.
25. Foster J.B. Evolution of mammals on islands. Nature 1964, 202:234-235.
26. Gordon A.D., Nevell L., Wood B. The Homo floresiensis cranium (LB1): size, scaling, and early Homo affinities. Proc. Natl. Acad. Sci. 2008, 105:4650-4655.
27. Gould S.J. Allometry in primates, with emphasis on scaling and the evolution of the brain. Contrib. Primatol. 1975, 5:244-292.
28. Harvey P.H., Pagel M.D. The Comparative Method in Evolutionary Biology 1991, Oxford University Press, Oxford.
29. Hershkovitz I., Kornreich L., Laron Z. Comparative skeletal features between Homo floresiensis and patients with primary growth hormone insensitivity (Laron syndrome). Am. J. Phys. Anthropol. 2008, 134:198-208.
30. Holloway R.L. Within-species brain-body weight variability: a reexamination of the Danish data and other primate species. Am. J. Phys. Anthropol. 1980, 53:109-121.
31. Holloway R., Schoenemann T., Monge J. The LB1 endocast: un-adorned, unsmoothed, a replication study based on the original CT scan data. Am. J. Phys. Anthropol. 2011, S52:165-166.
32. Irish J.D., Gautelli-Steinberg D., Legge S.S., de Ruiter D.J., Berger L.R. Dental morphology and the phylogenetic 'place' of Australopithecus sediba. Science 2013, 340. 10.1126/science.1233062.
33. Isler K., Kirk E.C., Miller J.M.A., Albrecht G.A., Gelvin B.R., Martin R.D. Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J.Hum. Evol. 2008, 55:967-978.
34. Jacob T., Indriati E., Soejono R.P., Hsu K., Frayer D.W., Eckhardt R.B., Kuperavage A.J., Thorne A., Henneberg M. Pygmoid Australomelanesian Homo sapiens skeletal remains from Liang Bua, Flores: population affinities and pathological abnormalities. Proc. Natl. Acad. Sci. 2006, 103:13421-13426.
35. Jerison H.J. Evolution of the Brain and Intelligence 1973, Academic Press, New York.
36. Jungers W.L., Harcourt-Smith W.E.H., Wunderlich R.E., Tocheri M.W., Larson S.G., Sutikna T., Due Awe R., Morwood M.J. The foot of Homo floresiensis. Nature 2009, 459:81-84.
37. Jungers W.L., Larson S.G., Harcourt-Smith W., Morwood M.J., Sutikna T., Due Awe R., Djubiantono T. Descriptions of the lower limb skeleton of Homo floresiensis. J.Hum. Evol. 2009, 57:538-554.
38. Kaifu Y., Baba H., Sutikna T., Morwood M.J., Kubo D., Saptomo E.W., Jatmiko, Awe D.R., Djubiantono T. Craniofacial morphology of Homo floresiensis: description, taxonomic affinities, and evolutionary implication. J.Hum. Evol. 2011, 61:644-682.
39. Kappelman J. The evolution of body mass and relative brain size in fossil hominids. J.Hum. Evol. 1996, 30:243.
40. Kimbel W.H. Hesitation on hominin history. Nature 2013, 497:573-574.
41. Köhler M., Moyá-Solá S. Reduction of brain and sense organs in the fossil insular bovid Myotragus. Brain Behav. Evol. 2004, 63:125-140.
42. Köhler M., Moyà-Solà S. Island rules cannot be broken. Trends Ecol. Evol. 2008, 23:6-7.
43. Kubo D., Kono R.T., Kaifu Y. Brain size of Homo floresiensis and its evolutionary implications. Proc. Roy. Soc. B 2013, 280. 10.1098/rspb.2013.0338.
44. Lande R. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 1979, 33:402-416.
45. Larson S.G., Jungers W.L., Morwood M.J., Sutikna T., Jatmiko, Saptomo E.W., Due R.A., Djubiantono T. Homo floresiensis and the evolution of the hominin shoulder. J.Hum. Evol. 2007, 53:718-731.
46. Lieberman D.E. Homo floresiensis from head to toe. Nature 2009, 459:41-42.
47. Lomolino M.V. Body size of mammals on islands: the island rule reexamined. Am. Nat. 1985, 125:310-316.
48. Lordkipanidze D., Jashashvili T., Vekua A., Ponce de León M.S., Zollikofer C.P.E., Rightmire G.P., Pontzer H., Ferring R., Oms O., Tappen M., Bukhsianidze M., Agustí J., Kahlke R., Kiladze G., Martinez-Navarro B., Mouskhelishvili A., Nioradze M., Rook L. Postcranial evidence from early Homo from Dmanisi, Georgia. Nature 2007, 449:305-310.
49. Mace G.M., Eisenberg J.F. Competition, niche specialization and the evolution of brain size in the genus Peromyscus. Biol. J. Linn. Soc. 1982, 17:243-257.
50. Martin R.D., MacLarnon A.M., Phillips J.L., Dussubieux L., Williams P.R., Dobyns W.B. Comment on "the brain of LB1 Homo floresiensis". Science 2006, 312:999.
51. Martinez A.M., Hamsici O.C. Who is LB1? Discriminate analysis for the classification of specimens. Pattern Recogn. 2008, 41:3436-3441.
52. McClain C.R., Durst P.A.P., Boyer A.G., Francis C.D. Unraveling the determinants of insular body size shifts. Biol. Lett. 2013, 9. 10.1098/rsbl.2012.0989.
53. Meijer H.J.M., van den Hoek Ostende L.W., van den Bergh G.D., de Vos J. The fellowship of the hobbit: the fauna surrounding Homo floresiensis. J.Biogeogr. 2010, 37:995-1006.
54. Meiri S., Dayan T., Simberloff D. The generality of the island rule reexamined. J.Biogeogr. 2006, 33:1571-1577.
55. Meiri S., Cooper N., Purvis A. The island rule: made to be broken?. Proc. Roy. Soc. B 2008, 275:141-148.
56. Meiri S., Raia P., Phillimore A.B. Slaying dragons: limited evidence for unusual body size evolution on islands. J.Biogeogr. 2011, 38:89-100.
57. Montgomery S.H., Mundy N.I. Parallel episodes of phyletic dwarfism in callitrichid and cheirogaleid primates. J.Evol. Biol. 2013, 26:810-819.
58. Montgomery S.H., Capellini I., Barton R.A., Mundy N.I. Reconstructing the ups and downs of primate brain evolution: implications for adaptive hypotheses and Homo floresiensis. BMC Biol. 2010, 8. 10.1186/1741-7007-8-9.
59. Morwood M.J., Brown P., Jatmiko, Sutikna T., Saptomo E.W., Westaway K.E., Due R.A., Roberts R.G., Maeda T., Wasisto S., Djubiantono T. Further evidence for small-bodied hominins from the Late Pleistocene of Flores, Indonesia. Nature 2005, 437:1012-1017.
60. Navarrete A., van Schaik C.P., Isler K. Energetics and the evolution of human brain size. Nature 2011, 480:91-93.
61. Niven J.E. Brains, islands and evolution: breaking all the rules. Trends Ecol. Evol. 2007, 22:57-59.
62. Oxnard C., Obendorf P.J., Kefford B.J. Post-cranial skeletons of hypothyroid cretins show a similar anatomical mosaic as Homo floresiensis. PLoS ONE 2010, 5:e13018.
63. Pagel M. Inferring the historical patterns of biological evolution. Nature 1999, 401:877-884.
64. Perelman P., Johnson W.E., Roos C., Seuánez H.N., Horvath J.E., Moreira M.A.M., Kessing B., Pontius J., Roelke M., Rumpler Y., Schneider M.P.C., Silva A., O'Brien S.J., Pecon-Slattery J. Amolecular phylogeny of living primates. PLoS Genet. 2011, 7:e1001342.
65. Peters M., Jäncke K., Staigner J.F., Schlaug G., Huang Y., Steinmetz H. Unsolved problems in comparing brain sizes in Homo sapiens. Brain Cogn. 1998, 37:254-285.
66. Pilbeam D., Gould S.J. Size and scaling in human evolution. Science 1974, 186:892-901.
67. Price T.D., Phillimore A.B. Reduced major axis regression and the island rule. J.Biogeogr. 2007, 34:1998-1999.
68. Reader S.M., Laland K.N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl. Acad. Sci. 2002, 99:4436-4441.
69. Rightmire G.P., Lordkipanidze D., Vekua A. Anatomical descriptions, comparative studies and evolutionary significance of the hominin skulls from Dmanisi, Republic of Georgia. J.Hum. Evol. 2006, 50:115-141.
70. Robson S.L., Wood B. Hominin life history: reconstruction and evolution. J.Anat. 2008, 212:394-425.
71. Roth V.L. Inferences from allometry and fossils: dwarfing of elephants on islands. Oxford Surv. Evol. Biol. 1992, 8:259-288.
72. Schillaci M.A., Meijaard E., Clark T. The effect of island area on body size in a primate species from the Sunda Shelf Islands. J.Biogeogr. 2009, 36:362-371.
73. Sol D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 2009, 5:130-133.
74. Stanyon R., Consigliere S., Morescalchi M.A. Cranial capacity in hominid evolution. Hum. Evol. 1993, 8:205.
75. Taylor A.B., van Schaik C.P. Variation in brain size and ecology in Pongo. J.Hum. Evol. 2007, 52:59-71.
76. Tocheri M.W., Orr C.M., Larson S.G., Sutikna T., Jatmiko, Saptomo E.W., Due W.A., Djubiantono T., Morwood M.J., Jungers W.L. The primitive wrist of Homo floresiensis and its implications for hominin evolution. Science 2007, 317:1743-1745.
77. Trueman J.W. Anew cladistic analysis of Homo floresiensis. J.Hum. Evol. 2010, 59:223-226.
78. Uhl N.M., Rainwater C.W., Konigsberg L.W. Testing for size and allometric differences in fossil hominin body mass estimation. Am. J. Phys. Anthropol. 2013, 151:215-229.
79. van Heteren A.H. Homo floresiensis as an island form. Palarch's J. Vertebr. Palaeontol. 2008, 5:1-19.
80. van Heteren A.H. The hominins of Flores: insular adaptations of the lower body. C.R. Palevol. 2012, 11:169-179.
81. Van Valen L. Pattern and the balance of nature. Evol. Theory 1973, 1:31-49.
82. van Woerden J.T., van Schaik C.P., Isler K. Effects of seasonality on brain size evolution: evidence from strepsirrhine primates. Am. Nat. 2010, 176:758-767.
83. van Woerden J.T., Willems E.P., van Schaik C.P., Isler K. Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution 2012, 66:191-199.
84. Vekua A., Lordkipanidze D., Rightmire G.P., Agustí J., Ferring R., Maisuradze G., Mouskhelishvili A., Nioradze M., Ponce de León M., Tappen M., Tvalchredlidze M., Zollikofer C. Anew skull of early Homo from Dmanisi, Georgia. Science 2002, 297:85-89.
85. Warton D.I., Ormerod J. Smatr Package, V. 2.1 2007, http://web.maths.unsw.edu.au/%7Edwarton.
86. Welch J.J. Testing the island rule: primates as a case study. Proc. Roy. Soc. B 2009, 276:675-682.
87. Weston E.M., Lister A.M. Insular dwarfism in hippos and a model for brain size reduction in Homo floresiensis. Nature 2009, 459:85-88.
88. Wood B. Did early Homo migrate 'out of' or 'in to' Africa?. Proc. Natl. Acad. Sci. 2011, 108:10375-10376.
89. Wood B., Collard M. The human genus. Science 1999, 284:65-71.
90. Wood B., Harrison T. The evolutionary context of the first hominins. Nature 2011, 470:347-352.