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Insular dwarfism in hippos and a model for brain size reduction in Homo floresiensis

Abstract

Body size reduction in mammals is usually associated with only moderate brain size reduction, because the brain and sensory organs complete their growth before the rest of the body during ontogeny1,2. On this basis, ‘phyletic dwarfs’ are predicted to have a greater relative brain size than ‘phyletic giants’1,3. However, this trend has been questioned in the special case of dwarfism of mammals on islands4. Here we show that the endocranial capacities of extinct dwarf species of hippopotamus from Madagascar are up to 30% smaller than those of a mainland African ancestor scaled to equivalent body mass. These results show that brain size reduction is much greater than predicted from an intraspecific ‘late ontogenetic’ model of dwarfism in which brain size scales to body size with an exponent of 0.35. The nature of the proportional change or grade shift2,5 observed here indicates that selective pressures on brain size are potentially independent of those on body size. This study demonstrates empirically that it is mechanistically possible for dwarf mammals on islands to evolve significantly smaller brains than would be predicted from a model of dwarfing based on the intraspecific scaling of the mainland ancestor. Our findings challenge current understanding of brain–body allometric relationships in mammals and suggest that the process of dwarfism could in principle explain small brain size, a factor relevant to the interpretation of the small-brained hominin found on the Island of Flores, Indonesia6.

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Figure 1: Relationship between brain size and cranial size for an intraspecific ‘late ontogenetic’ model of dwarfing.
Figure 2: Relationship between brain size and cranial size for an intraspecific ‘ontogenetic’ model of dwarfing.

References

  1. Shea, B. T. Phyletic size change and brian/body allometry: a consideration based on the African pongids and other primates. Int. J. Primatol. 4, 33–62 (1983)

    Article  Google Scholar 

  2. Martin, R. D. Human Brain Evolution in an Ecological Context: 52nd James Arthur Lecture on the Evolution of the Human Brain (American Museum of Natural History, New York, 1983)

    Google Scholar 

  3. Gould, S. J. Allometry in primates with emphasis on scaling and the evolution of the brain. Contrib. Primatol. 5, 244–292 (1975)

    CAS  PubMed  Google Scholar 

  4. Köhler, M. & Moyà-Solà, S. Reduction of brain and sense organs in the fossil insular bovid Myotragus . Brain Behav. Evol. 63, 125–140 (2004)

    Article  Google Scholar 

  5. Martin, R. D. & Harvey, P. H. in Size and Scaling in Primate Biology (ed. Jungers, W. L.) 147–173 (Plenum, 1985)

    Book  Google Scholar 

  6. Brown, P. et al. A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431, 1055–1061 (2004)

    Article  ADS  CAS  Google Scholar 

  7. Niven, J. E. Brains, islands and evolution: breaking all the rules. Trends Ecol. Evol. 22, 57–59 (2006)

    Article  Google Scholar 

  8. Richards, G. D. Genetic, physiologic and ecogeographic factors contributing to variation in Homo sapiens: Homo floresiensis reconsidered. J. Evol. Biol. 19, 1744–1767 (2006)

    Article  CAS  Google Scholar 

  9. Lalueza-Fox, C., Shapiro, B., Bover, P., Alcover, J. A. & Bertranpetit, J. Molecular phylogeny and evolution of the extinct bovid Myotragus balearicus . Mol. Phylogenet. Evol. 25, 501–510 (2002)

    Article  CAS  Google Scholar 

  10. Martin, R. D. et al. Comment on ‘The brain of LB1, Homo floresiensis’. Science 312, 999b (2006)

    Article  Google Scholar 

  11. Martin, R. D., Maclarnon, A. M., Phillips, J. L. & Dobyns, W. B. Flores hominid: new species or microcephalic dwarf? Anat. Rec. 288A, 1123–1145 (2006)

    Article  Google Scholar 

  12. Köhler, M., Moyà-Solà, S. & Wrangham, R. W. Island rules cannot be broken. Trends Ecol. Evol. 23, 6–7 (2008)

    Article  Google Scholar 

  13. Argue, D., Donlon, D., Groves, C. & Wright, R. Homo floresiensis: microcephalic, pygmoid, Australopithecus, or Homo? J. Hum. Evol. 51, 360–374 (2006)

    Article  Google Scholar 

  14. Niven, J. E. Response to Köhler et al. Impossible arguments about possible species? Trends Ecol. Evol. 23, 8–9 (2008)

    Article  Google Scholar 

  15. Lande, R. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution Int. J. Org. Evolution 33, 402–416 (1979)

    Article  Google Scholar 

  16. Kruska, D. C. T. On the evolutionary significance of encephalization in some eutherian mammals: effects of adaptive radiation, domestication and feralization. Brain Behav. Evol. 65, 73–108 (2005)

    Article  Google Scholar 

  17. Stuenes, S. Taxonomy, habits, and relationships of the subfossil Madagascan hippopoptami Hippopotamus lemerlei and H. madagascariensis . J. Vertebr. Paleontol. 9, 241–268 (1989)

    Article  Google Scholar 

  18. Boisserie, J.-R. The phylogeny and taxonomy of Hippopotamidae (Mammalia: Artiodactyla): a review based on morphology and cladistic analysis. Zool. J. Linn. Soc. 143, 1–26 (2005)

    Article  Google Scholar 

  19. Eltringham, S. K. The Hippos: Natural History and Conservation (Academic, 1999)

    Google Scholar 

  20. Burney, D. A. et al. A chronology for late prehistoric Madagascar. J. Hum. Evol. 47, 25–63 (2004)

    Article  Google Scholar 

  21. Weston, E. M. Evolution of ontogeny in the hippopotamus skull: using allometry to dissect developmental change. Biol. J. Linn. Soc. 80, 625–638 (2003)

    Article  Google Scholar 

  22. Accordi, F. S. & Palombo, M. R. Morfologia endocranica degli elefanti nani pleistocenici di Spinagallo (Siracusa) e comparazione con l’ endocranio di Elephas antiquus . Atti Accad. Naz. Lincei Rc. 51, 111–124 (1971)

    Google Scholar 

  23. Roth, V. L. Inferences from allometry and fossils: dwarfing of elephants on islands. Oxf. Surv. Evol. Biol. 8, 259–288 (1992)

    Google Scholar 

  24. Shoshani, J., Kupsky, W. J. & Marchant, G. H. Elephant brain. Part I: Gross morphology, functions, comparative anatomy, and evolution. Brain Res. Bull. 70, 124–157 (2006)

    Article  Google Scholar 

  25. Christiansen, P. Body size in proboscideans, with notes on elephant metabolism. Zool. J. Linn. Soc. 140, 524–549 (2004)

    Article  Google Scholar 

  26. Kappelman, J. The evolution of body mass and relative brain size in fossil hominids. J. Hum. Evol. 30, 243–276 (1996)

    Article  Google Scholar 

  27. Stanyon, R., Consigliere, S. & Morescalchi, M. A. Cranial capacity in hominid evolution. Hum. Evol. 8, 205–216 (1993)

    Article  Google Scholar 

  28. Jacob, T. et al. Pygmoid Australomelanesian Homo sapiens skeletal remains from Liang Bua, Flores: population affinities and pathological abnormalities. Proc. Natl Acad. Sci. USA 103, 13421–13426 (2006)

    Article  ADS  CAS  Google Scholar 

  29. Lordkipanidze, D. et al. A fourth hominin skull from Dmanisi, Georgia. Anat. Rec. 288A, 1146–1157 (2006)

    Article  Google Scholar 

  30. Lordkipanidze, D. et al. Postcranial evidence from early Homo from Dmanisi, Georgia. Nature 449, 305–310 (2007)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank A. Currant, C. Lefèvre, C. Sagne, E. Gilissen, F. Renoult, H. Chatterjee, J. Ashby, M. Nowak-Kemp, M. Harman, P. Jenkins, P. Tassy, R. Sabin, R. Symonds and S. Stuenes for facilitating access to museum collections; A. Rasoamiaramanana, G. Ravololonarivo, H. Andriamialison, T. Rakotondrazafy, M. Ramarolahy and S. Bourlat for permission and/or assistance with study of the subfossil material held in the University of Antananarivo and the Académie Malagache; B. Ramanivosoa, D. Gommery, C. Guérin and M. Faure for allowing the study of material at the Akiba Museum, Mahajanga, Madagascar; R. Portela Miguez for assistance with recording endocranial capacity measures from H. amphibius specimens in the Natural History Museum, London; A. Friday for assistance with data collection in the University Museum of Zoology, Cambridge; C. Anderung, J.-R. Boisserie, S. Walsh and V. Herridge for discussion and helpful comments; and J. Kappelman, J. Niven, D. Lieberman and A. Gordon for comments on earlier versions of this manuscript. This research was supported by the Biotechnology and Biological Sciences Research Council.

Author Contributions E.W. and A.L. designed the study. E.W. collected and analysed the data and drafted the paper. Both authors discussed the results and edited the manuscript.

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Correspondence to Eleanor M. Weston.

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Weston, E., Lister, A. Insular dwarfism in hippos and a model for brain size reduction in Homo floresiensis. Nature 459, 85–88 (2009). https://doi.org/10.1038/nature07922

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