From Jumbo to Dumbo: Cranial Shape Changes in Elephants and Hippos During Phyletic Dwarfing
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.
KeywordsEvolution Geometric morphometrics Insular dwarf species Pedomorphism Pleistocene
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.
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.
- 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
- 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
- Aguirre, E. (1969). Revision sistematica de los Elephantidae, por su morfologia y morfometria dentaria. Estudios Geologicos, 25, 317–367.Google Scholar
- Ambrosetti, P. (1968). The Pleistocene dwarf elephant of Spinagallo. Geologica Romana, 7, 277–398.Google Scholar
- 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
- 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
- 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
- Dryden, I. L., & Mardia, K. M. (2008). Statistical shape analysis. Chicester: Wiley.Google Scholar
- Goodman, S. M., & Jungers, W. L. (2014). Extinct Madagascar: Picturing the Island’s Past. Chicago: University of Chicago Press.Google Scholar
- Herridge, V. L. (2010). Dwarf elephants on Mediterranean islands: A natural experiment in parallel evolution. PhD Thesis, University College, London.Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- Roth, V. L. (1992). Inferences from allometry and fossils: Dwarfing of elephants on islands. Oxford Surveys in Evolutionary Biology, 8, 259–288.Google Scholar
- 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
- Smaers, J. B. (2014). Evomap: R-package for the evolutionary mapping of continuous traits. Available at Github: https://github.com/JeroenSmaers/evomap.
- 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
- 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
- van Heteren, A. H. (2008). Homo floresiensis is an island form. PalArch’s Journal of Vertebrate Palaeonotology, 5(2), 1–12.Google Scholar
- Weston, E. M. (1998). A biometrical analysis of evolutionary change within the Hippopotamidae. PhD thesis, University of Cambridge, England.Google Scholar