Advertisement

Evolutionary Biology

, Volume 45, Issue 3, pp 303–317 | Cite as

From Jumbo to Dumbo: Cranial Shape Changes in Elephants and Hippos During Phyletic Dwarfing

  • Alexandra A. E. van der Geer
  • George A. Lyras
  • Philipp Mitteroecker
  • Ross D. E. MacPhee
Research Article

Abstract

Members of the mammalian families Elephantidae and Hippopotamidae (extant and extinct elephants and hippos) include extinct dwarf species that display up to 98% decrease in body size compared to probable ancestral sources. In addition to differences in body mass, skulls of these species consistently display distinctive morphological changes, including major reduction of pneumatised areas in dwarf elephants and shortened muzzles in dwarf hippos. Here we build on previous studies of island dwarf species by conducting a geometric morphometric analysis of skull morphology and allometry in target taxa, living and extinct, and elaborate on the relation between skull size and body size. Our analysis indicates that skull size and body size within terrestrial placental mammals scale almost isometrically (PGLS major axis slope 0.906). Furthermore, skull shape in dwarf species differed from both their ancestors and the juveniles of extant species. In insular dwarf hippos, the skull was subject to considerable anatomical reorganisation in response to distinct selection pressures affecting early ontogeny (the “island syndrome”). By contrast, skull shape in adult insular dwarf elephants can be explained well by allometric effects; selection on size may thus have been the main driver of skull shape in dwarf elephants. We suggest that a tightly constrained growth trajectory, without major anatomical reorganization of the skull, allowed for flexible adaptations to changing environments and was one of the factors underlying the evolutionary success of insular dwarf elephants.

Keywords

Evolution Geometric morphometrics Insular dwarf species Pedomorphism Pleistocene 

Notes

Acknowledgements

We thank Steven van der Mije and Wendy van Bohemen (RMNH), Eileen Westwig and Neil Duncan (AMNH), Laurence Heaney and the late William Stanley (FMNH), Carolina di Patti (MGG), Oliver Hampe, Frieder Mayer and Nora Lange (MFN), Christine Argot and Christine Lefèvre (MNHN), Rainer Brocke and Christine Hertler (SFN), Reinhard Ziegler (SMNS), Darrin Lunde and Nicole Edmison (USNM), Chloe Adamopoulou (ZMUA), Pasquale Raia and Mariella Del Re (MPUN) and Pip Brewer (Natural History Museum, London) for allowing us to study the skulls in their care and their assistance when skulls were too heavy to handle two-handed. We further thank Rutger Vos for clarifying PGLS regressions, and Gert van den Bergh (Centre for Archaeological Science, University of Wollongong), Maria Rita Palombo (‘La Sapienza’ University of Rome), Athanassios Athanassiou (Hellenic Ministery of Culture), Adrian Lister, Chris Stringer and Victoria Herridge (Natural History Museum, London) for discussions we had on island dwarfs.

Funding

GL received support from the SYNTHESYS Project (GB-TAF-6355 and FR-TAF-6549). The research of AVDG has been co-financed by the European Union (European Social Fund—ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF)—Research Funding Program: THALIS—UOA-Island biodiversity and cultural evolution: examples from the Eastern Mediterranean, Madagascar, Mauritius and Philippines during the past 800,000 years (MIS375910, KA:70/3/11669).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11692_2018_9451_MOESM1_ESM.doc (60 kb)
Supplementary material 1 (DOC 60 KB)

References

  1. Accordi, F. S., & Palombo, M. R. (1971). Morfologia endocranica degli elephanti nani pleistocenici de Spinagalo (Siracusa) e comparazione con l´endocranio de Elephas antiquus. Rediconti dell´Accademia Nazionale del Lincei (Series 8), 51, 111–124.Google Scholar
  2. Adam, K. D. (1986). Fossilfunde aus den Cannstatter Sauerwasserkalken. In K. D. Adam, W. Reif & E. Wagner (Eds.), Seugnisse des Urmenschen aus den Cannstatter Sauerwasserkalken (Vol. 11, pp. 25–61). Baden-Württemberg: Fundber.Google Scholar
  3. Aguirre, E. (1969). Revision sistematica de los Elephantidae, por su morfologia y morfometria dentaria. Estudios Geologicos, 25, 317–367.Google Scholar
  4. Ambrosetti, P. (1968). The Pleistocene dwarf elephant of Spinagallo. Geologica Romana, 7, 277–398.Google Scholar
  5. Argue, D., Donlon, D., Groves, C., & Wright, R. (2006). Homo floresiensis: Microcephalic, pygmoid, Australopithecus or Homo? Journal of Human Evolution, 51, 360–374.CrossRefPubMedGoogle Scholar
  6. Argue, D., Groves, C. P., Lee, M. S. Y., & Jungers, W. L. (2017). The afffinities of Homo floresiensis based on phylogenetic analyses of cranial, dental, and postcranial characters. Journal of Human Evolution, 197, 107–133.CrossRefGoogle Scholar
  7. Argue, D., Morwood, M., Sutikna, T., Jatmiko, W., & Saptomo, E. (2009). Homo floresiensis: A cladistic analysis. Journal of Human Evolution, 57, 623–639.CrossRefPubMedGoogle Scholar
  8. Athanassiou, A., Herridge, V., Reese, D. S., et al. (2015). Cranial evidence for the presence of a second endemic elephant species on Cyprus. Quaternary International, 379, 47–57.CrossRefGoogle Scholar
  9. Baab, K. L., & McNulty, K. P. (2009). Size, shape, and asymmetry in fossil hominins: The status of the LB1 cranium based on 3D morphometric analyses. Journal of Human Evolution, 57, 608–622.CrossRefPubMedGoogle Scholar
  10. 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. (2007). The delayed rise of present-day mammals. Nature, 446, 507–512.CrossRefPubMedGoogle Scholar
  11. Boekschoten, G. J., & Sondaar, P. Y. (1972). On the fossil mammalia of Cyprus, I and II. Proceedings van de Koninklijke Nederlandse Akademie van Wetenschappen, 75, 306–338.Google Scholar
  12. Boisserie, J. R. (2005). The phylogeny and taxonomy of Hippopotamidae (Mammalia: Artiodactyla): A review based on morphology and cladistic analysis. Zoological Journal of the Linnean Society, 143, 1–26.CrossRefGoogle Scholar
  13. Cardini, A., & Polly, P. D. (2013). Larger mammals have longer faces because of size-related constraints on skull form. Nature Communications, 4, 2458.  https://doi.org/10.1038/ncomms3458.CrossRefPubMedGoogle Scholar
  14. Chiozzi, G., Bardelli, G., Ricci, M., De Marchi, G., & Cardini, A. (2014). Just another island dwarf? Phenotypic distinctiveness in the poorly known Soemmerring’s Gazelle, Nanger soemmerringii (Cetartiodactyla: Bovidae), of Dahlak Kebir Island. Biological Journal of the Linnean Society, 111, 603–620.CrossRefGoogle Scholar
  15. Coryndon, S. C. (1977). The taxonomy and nomenclature of the Hippopotamidae (Mammalia, Artiodactyla) and a description of two new fossil species. The nomenclature of the Hippopotamidae. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen B, 80, 61–88.Google Scholar
  16. Dryden, I. L., & Mardia, K. M. (2008). Statistical shape analysis. Chicester: Wiley.Google Scholar
  17. Evans, A. R., Jones, D., Boyer, A. G., et al. (2012). The maximum rate of mammal evolution. Proceedings of the National Academy of Sciences of the United States of America, 109, 4187–4190.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Falk, D., Hildebolt, C., Smith, K., et al. (2007). Brain shape in human microcephalics and Homo floresiensis. Proceedings of the National Academy of Sciences of the USA, 104, 2513–2518.CrossRefPubMedGoogle Scholar
  19. Ferretti, M. P. (2008). The dwarf elephant Palaeoloxodon mnaidriensis from Puntali Cave, Carini (Sicily; late Middle Pleistocene): Anatomy, systematics and phylogenetic relationships. Quaternary International, 182, 90–108.CrossRefGoogle Scholar
  20. Fovet, W., Faure, M., & Guerin, C. (2011). Hippopotamus guldbergi n. sp.: révision du statut d'Hippopotamus madagascariensis Guldberg, 1883, après plus d'un siècle de malentendus et deconfusions taxonomiques. Zoosystema, 33, 61–82.CrossRefGoogle Scholar
  21. Goodman, S. M., & Jungers, W. L. (2014). Extinct Madagascar: Picturing the Island’s Past. Chicago: University of Chicago Press.Google Scholar
  22. Herridge, V. L. (2010). Dwarf elephants on Mediterranean islands: A natural experiment in parallel evolution. PhD Thesis, University College, London.Google Scholar
  23. Houtekamer, J. L., & Sondaar, P. Y. (1979). Osteology of the fore limb of the Pleistocene dwarf hippopotamus from Cyprus with special reference to phylogeny and function. Proceedings van de Koninklijke Nederlandse Akademie van Wetenschappen, 82, 411–448.Google Scholar
  24. Iinuma, Y. M., Tanaka, S., Kawasaki, K., Kuwajima, T., Nomura, H., Suzuki, M., & Ohtaishi, N. (2004). Dental incremental lines in Sika Deer (Cervus nippon); polarized light and fluorescence microscopy of ground sections. Journal of Veterinary Medical Science, 66, 665–669.CrossRefPubMedGoogle Scholar
  25. Kaifu, Y., Baba, H., Sutika, T., Morwood, M. J., Kubo, D., Saptomo, W., Jatmiko, E., Due Awe, R., & Djubiantono, T. (2011). Craniofacial morphology of Homo floresiensis: Description, taxonomic affinities, and evolutionary implication. Journal of Human Evolution, 61, 644–682.CrossRefPubMedGoogle Scholar
  26. Katsikosta, N., & Theodorou, G. (1994). Conservation and reconstruction of a juvenile skull of Palaeoloxodon antiquus falconeri from Charkadio Cave, Tilos island (Dodecanese, Greece). Bulletin of the Speleological Society of Greece, 21, 263–628.Google Scholar
  27. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.CrossRefPubMedGoogle Scholar
  28. Kolb, C., Scheyer, T. M., Veitschegger, K., et al. (2015). Mammalian bone palaeohistology: A survey and new data with emphasis on island forms. PeerJ, 3, e1358.  https://doi.org/10.7717/peerj.1358.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kubo, M. O., Fujita, M., Matsu’ura, S., Kondo, M., & Suwa, G. (2011). Mortality profiles of late Pleistocene deer remains of Okinawa Island: Evidence from the Hananda-Gama cave and Yamashita-cho cave I sites. Anthropological Series, 119, 183–201.CrossRefGoogle Scholar
  30. Kurt, F., & Kumarasinghe, J. C. (1998). Remarks on body growth and phenotypes in Asian elephant Elephas maximus. Acta Theriologica, 43, 135–153.CrossRefGoogle Scholar
  31. Laws, R. M. (1966). Age criteria for the African elephant Loxodonta africana. East African Wildlife Journal, 4, 1–37.CrossRefGoogle Scholar
  32. Laws, R. M. (1968). Dentition and ageing of the Hippopotamus. East African Wildlife Journal, 6, 19–52.CrossRefGoogle Scholar
  33. Lister, A. M. (1989). Rapid dwarfing of red deer on Jersey in the Last Interglacial. Nature, 342, 539–542.CrossRefPubMedGoogle Scholar
  34. Lister, A. M. (1996). Dwarfing in island elephants and deer: Processes in relation to time of isolation. Symposia of the Zoological Society of London, 69, 277–292.Google Scholar
  35. Lomolino, M. V., Sax, D. F., Palombo, M. R., & van der Geer, A. A. E. (2012). Of Mice and mammoths: Evaluations of causal explanations for body size evolution in insular mammals. Journal of Biogeography, 39, 842–854.CrossRefGoogle Scholar
  36. Lomolino, M. V., van der Geer, A. A. E., Lyras, G. A., Palombo, M. R., Sax, D. F., & Rozzi, R. (2013). Of mice and mammoths: Generality and antiquity of the island rule. Journal of Biogeography, 40, 1427–1439.CrossRefGoogle Scholar
  37. Lyras, G. A., Dermitzakis, M. D., van der Geer, A. A. E., & de Vos, J. (2009). The origin of Homo floresiensis and its relation to evolutionary processes under isolation. Anthropological Science, 117, 33–43.CrossRefGoogle Scholar
  38. Lyras, G. A., van der Geer, A. A. E., & Rook, L. (2010). Body size of insular carnivores: Evidence from the fossil record. Journal of Biogeography, 37, 1007–1021.CrossRefGoogle Scholar
  39. Lyras, G. A., van der Geer, A. E., Dermitzakis, M., & de Vos, J. (2006). Cynotherium sardous, an insular canid (Mammalia: Carnivora) from the Pleistocene of Sardinia (Italy), and its origin. Journal of Vertebrate Paleontology, 26, 735–745.CrossRefGoogle Scholar
  40. Martin, R. B. (2005). The Transboundary Mammal Project of the Ministry of Environment and Tourism, Namibia (p. 74). Windhoek: The Namibia Nature Foundation.Google Scholar
  41. Martinez, A., & Hamsici, O. (2008). Who is LB1? Discriminant analysis for the classification of specimens. Pattern Recognition, 41, 3436–3441.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Masters, J. C., Génin, F., Silvestro, D., Lister, A. M., & DelPero, M. (2014). The red island and the seven dwarfs: Body size reduction in Cheirogaleidae. Journal of Biogeography, 41, 1833–1847.CrossRefGoogle Scholar
  43. Millien, V. (2006). Morphological evolution is accelerated among island mammals. PLoS Biology, 4, e321.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mitteroecker, P., Gunz, P., & Bookstein, F. L. (2005). Heterochrony and geometric morphometrics: A comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evolution & Development, 7, 244–258.CrossRefGoogle Scholar
  45. Mitteroecker, P., Gunz, P., Windhager, S., & Schaefer, K. (2013). A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix, The Italian Journal of Mammalogy, 24, 59–66.Google Scholar
  46. O’Higgins, P., & Jones, N. (1998). Morphologika a program for the analysis of 3-dimensional shape variation using landmarks. http://discovery.ucl.ac.uk/id/eprint/172805.
  47. Palkopoulou, E., Lipson, M., Mallick, S., Nielsen, S., Rohland, N., Baleka, S., et al. (2018). A comprehensive genomic history of extinct and living elephants. Proceedings of the National Academy of Sciences of the USA.  https://doi.org/10.1073/pnas.1720554115.PubMedGoogle Scholar
  48. Palombo, M. R. (2001). Paedomorphic features and allometric growth in the skull of Elephas falconeri from Spinagallo (Middle Pleistocene, Sicily). In G. Cavaretta, P. Gioia, M. Mussi & M. R. Palombo (Eds), The World of Elephants. Proceedings of the First International Congress, Rome, (Vol. 16–20, pp. 492–496). Roma: CNR.Google Scholar
  49. Penin, X., Berge, C., & Baylac, M. (2002). Ontogenetic study of the skull in modern humans and the common chimpanzees: Neotenic hypothesis reconsidered with a tridimensional procrustes analysis. American Journal of Physical Anthropology, 118, 50–62.CrossRefPubMedGoogle Scholar
  50. Pergams, O. R. W., & Ashley, M. V. (1999). Rapid morphological change in island deer mice. Evolution, 53, 1573–1581.CrossRefPubMedGoogle Scholar
  51. Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63, 3258–3268.CrossRefPubMedGoogle Scholar
  52. Roca, A. L., Georgiadis, N., Pecon-Slattery, J., & O’Brien, S. J. (2001). Genetic evidence for two species of elephant in Africa. Science, 293, 1473–1477.CrossRefPubMedGoogle Scholar
  53. Roth, V. L. (1984). How elephants grow: Heterochrony and the calibration of developmental stages in some living and fossil species. Journal of Vertebrate Paleontology, 4, 126–145.CrossRefGoogle Scholar
  54. Roth, V. L. (1992). Inferences from allometry and fossils: Dwarfing of elephants on islands. Oxford Surveys in Evolutionary Biology, 8, 259–288.Google Scholar
  55. Roth, V. L. (1993). Dwarfism and variability in the Santa Rosa Island mammoth (Mammuthus exilis): An interspecific comparison of limb-bone sizes and shapes in elephants. In F. G. Hochberg (Ed.), Third California Islands Symposium (pp. 433–442). Santa Barbara: Santa Barbara Museum of Natural History.Google Scholar
  56. Roth, V. L., & Shoshani, J. (1988). Dental identification and age determination in Elephas maximus. Journal of Zoology, 214, 288–567.CrossRefGoogle Scholar
  57. Sikes, K. S. (1967). The African elephant, Loxodonta africana: A field method for the estimation of age. Journal of Zoology, 154, 235–248.CrossRefGoogle Scholar
  58. Smaers, J. B. (2014). Evomap: R-package for the evolutionary mapping of continuous traits. Available at Github: https://github.com/JeroenSmaers/evomap.
  59. Smith, F. A., Lyons, S. K., Ernest, S. K. M., Jones, K. E., Kaufman, D. M., Dayan, T., Marquet, P. A., Brown, J. H., & HaskelI, J. P. (2003). Body mass of late Quaternary mammals. Ecology, 84, 3402.CrossRefGoogle Scholar
  60. Sondaar, P. Y. (1977). Insularity and its effect on mammal evolution. In M. K. Hecht, P. C. Goody & B. M. Hecht (Eds), Major Patterns in Vertebrate Evolution (pp. 671–707). New York: Plenum Publications Corporation.CrossRefGoogle Scholar
  61. Sondaar, P. Y. (1994). Paleoecology and evolutionary patterns in horses and island mammals. Historical Biology, 8, 1–13.CrossRefGoogle Scholar
  62. Stuenes, S. (1989). Taxonomy, habits, and relationships of the subfossil Madagascan Hippopotami Hippopotamus lemerlei and H. madagascariensis.. Journal of Vertebrate Paleontology, 9, 241–268.CrossRefGoogle Scholar
  63. Todd, N. (2010). Qualitative Comparison of the Cranio-Dental Osteology of the Extant Elephants, Elephas Maximus (Asian Elephant) and Loxodonta africana (African Elephant). The Anatomical Record, 293, 62–73.CrossRefPubMedGoogle Scholar
  64. van den Bergh, G. D., Kaifu, Y., Kurniawan, I., et al. (2016). Homo floresiensis-like fossils from the early Middle Pleistocene of Flores. Nature, 534, 245–248.CrossRefPubMedGoogle Scholar
  65. van den Bergh, G. D., Meijer, H. J. M., Awe, R. D. et al. (2009). The Liang Bua faunal remains: A 95k.yr. sequence from Flores, East Indonesia. Journal of Human Evolution, 57, 527–537.CrossRefPubMedGoogle Scholar
  66. van der Geer, A., Lyras, G., de Vos, J., & Dermitzakis, M. (2010). Evolution of Island Mammals: Adaptation and Extinction of Placental Mammals on Islands (p. 479). Oxford: Wiley-Blackwell Publishing.CrossRefGoogle Scholar
  67. van der Geer, A. A. E. (2005). Island ruminants and the evolution of parallel functional structures. In E. Crégut (Ed.) Les ongules holarctiques du Pliocene et du Pleistocene. Actes Colloque International Avignon, (Vol. 19–22, pp. 231–240) Quaternair (hors-serie 2).Google Scholar
  68. van der Geer, A. A. E. (2014). Parallel patterns and trends in functional structures in island mammals. Integrative Zoology, 9, 167–182.CrossRefGoogle Scholar
  69. van der Geer, A. A. E., Lyras, G. A., Lomolino, M. V., Palombo, & Sax, M. R., D.F (2013). Body size evolution of palaeo-insular mammals: Temporal variations and interspecific interactions. Journal of Biogeography, 40, 1440–1450.CrossRefGoogle Scholar
  70. van der Geer, A. A. E., Lyras, G. A., van den Hoek Ostende, L. W., de Vos, J., & Drinia, H. (2014). A dwarf elephant and a rock mouse on Naxos (Cyclades, Greece) with a revision of the palaeozoogeography of the Cycladic Islands (Greece) during the Pleistocene. Palaeogeography, Palaeoclimatology, Palaeoecology, 404, 133–144.CrossRefGoogle Scholar
  71. van der Geer, A. A. E., van den Bergh, G. D., Lyras, G. A., Prasetyo, U. W., Awe Due, R., Setiyabudi, E., & Drinia, H. (2016). The effect of area and isolation on insular dwarf proboscideans. Journal of Biogeography, 43, 1656–1666.CrossRefGoogle Scholar
  72. van Heteren, A. H. (2008). Homo floresiensis is an island form. PalArch’s Journal of Vertebrate Palaeonotology, 5(2), 1–12.Google Scholar
  73. Van Valen, L. (1973). Body size and numbers of plants and animals. Evolution, 27, 27–35.CrossRefPubMedGoogle Scholar
  74. Weston, E. M. (1998). A biometrical analysis of evolutionary change within the Hippopotamidae. PhD thesis, University of Cambridge, England.Google Scholar
  75. Weston, E. M. (2003). Evolution of ontogeny in the hippopotamus skull: Using allometry to dissect developmental change. Biological Journal of the Linnean Society, 80, 625–638.CrossRefGoogle Scholar
  76. Weston, E. M., & Lister, A. M. (2009). Insular dwarfism in hippos and a model for brain size reduction Homo floresiensis. Nature, 459, 85–88.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zeitoun, V., Barriel, V., & Widianto, H. (2016). Phylogenetic analysis of the calvaria of Homo floresiensis. Comptes Rendus Palevol, 15, 555–568.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Naturalis Biodiversity CenterLeidenThe Netherlands
  2. 2.Faculty of Geology and GeoenvironmentNational and Kapodistrian University of AthensAthensGreece
  3. 3.Department of Theoretical BiologyUniversity of ViennaViennaAustria
  4. 4.Division of Vertebrate Zoology (Mammalogy)American Museum of Natural HistoryNew YorkUSA

Personalised recommendations