Abstract
Among closely related species, larger mammals tend to have a longer face and proportionally smaller braincase. This putative ‘rule’ in mammalian macroevolution has been proposed for the first time in 2013 based on 3D geometric morphometrics of antelopes, fruit bats, tree squirrels and mongooses. To firmly demonstrate that this trend holds as a ‘rule’ requires expanding the analysis in more lineages and other mammalian orders: if supported in most groups, it may indeed become a new evolutionary ‘rule’ besides famous ones such as Bergmann’s and Allen’s. In this study, using statistical shape analysis and both standard and comparative methods on a sample of kangaroos, wallabies and other macropodine marsupials, we show that the ‘big size-long face’ pattern is indeed found also outside the placentals. This provides support to the hypothesis of an important role of size-related shape changes (i.e., allometry) in the origin of the exceptional disparity of mammals, that, only in terms of size, span more orders of magnitude than any other animal: from 3 to 4 g of a tiny bat to more than 100 tons in blue whales.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams, D. C., & Collyer, M. L. (2015). Permutation tests for phylogenetic comparative analyses of high-dimensional shape data: What you shuffle matters. Evolution. doi:10.1111/evo.12596.
Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10(1), 216.
Adams, D. C., & Otárola-Castillo, E. (2013). Geomorph: An r package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399.
Adams, D. C., Rohlf, F. J., & Slice, D. E. (2013). A field comes of age: Geometric morphometrics in the 21st century. Hystrix, the Italian Journal of Mammalogy, 24(1), 7–14.
Bennett, C. V., & Goswami, A. (2013). Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biology, 11(1), 52.
Black, K. H., Archer, M., Hand, S. J., & Godthelp, H. (2010). First comprehensive analysis of cranial ontogeny in a fossil marsupial—From a 15-million-year-old cave deposit in northern Australia. Journal of Vertebrate Paleontology, 30(4), 993–1011.
Cardini, A. (2013). Geometric morphometrics (in EOLSS encyclopedia of life support systems).
Cardini, A., & Elton, S. (2007). Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology, 126(2), 121–134. doi:10.1007/s00435-007-0036-2.
Cardini, A., & Elton, S. (2008). Does the skull carry a phylogenetic signal? Evolution and modularity in the guenons. Biological Journal of the Linnean Society, 93(4), 813–834.
Cardini, A., & Polly, P. D. (2013). Larger mammals have longer faces because of size-related constraints on skull form. Nature Communications,. doi:10.1038/ncomms3458.
Cardini, A., Seetah, K., & Barker, G. (2015). How many specimens do I need? Sampling error in geometric morphometrics: Testing the sensitivity of means and variances in simple randomized selection experiments. Zoomorphology,. doi:10.1007/s00435-015-0253-z.
Drake, A. G., & Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. The American Naturalist, 175(3), 289–301.
Emerson, S. B., & Bramble, D. M. (1993). Scaling, allometry, and skull design. The Skull, 3, 384–421.
Helgen, K. M., Wells, R. T., Kear, B. P., Gerdtz, W. R., & Flannery, T. F. (2006). Ecological and evolutionary significance of sizes of giant extinct kangaroos. Australian Journal of Zoology, 54(4), 293–303.
Janis, C. M., Buttrill, K., & Figueirido, B. (2014). Locomotion in extinct giant kangaroos: Were sthenurines hop-less monsters? PLoS ONE, 9(10), e109888.
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.
Klingenberg, C. P. (2013a). Visualizations in geometric morphometrics: How to read and how to make graphs showing shape changes. Hystrix, the Italian Journal of Mammalogy, 24(1), 15–24.
Klingenberg, C. P. (2013b). Cranial integration and modularity: Insights into evolution and development from morphometric data. Hystrix, the Italian Journal of Mammalogy, 24(1), 43–58.
Klingenberg, C. P., & Marugán-Lobón, J. (2013). Evolutionary covariation in geometric morphometric data: Analyzing integration, modularity, and allometry in a phylogenetic context. Systematic Biology, 62(4), 591–610.
Long, J. A. (2002). Prehistoric mammals of Australia and New Guinea: One hundred million years of evolution. Sydney: University of New South Wales press.
Maddison, W. P., & Maddison, D. (2001). Mesquite: A modular system for evolutionary analysis, ver. 1.0.
Meredith, R. W., Westerman, M., & Springer, M. S. (2009). A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences. Australian Journal of Zoology, 56(6), 395–410.
Merino, M. L., Milne, N., & Vizcaíno, S. F. (2005). A cranial morphometric study of deer (Mammalia, Cervidae) from Argentina using three-dimensional landmarks. Acta Theriologica, 50(1), 91–108.
Milne, N., & O’Higgins, P. (2002). Inter-specific variation in macropus crania: Form, function and phylogeny. Journal of Zoology, 256(04), 523–535.
Monteiro, L. R. (2013). Morphometrics and the comparative method: Studying the evolution of biological shape. Hystrix, the Italian Journal of Mammalogy, 24(1), 8–14.
O’Higgins, P., & Jones, N. (2006). Morphologika. Tools for statistical shape analysis. Hull York Medical School. http://sites.google.com/site/hymsfme/resources.
Polly, P. D. (2008). Adaptive zones and the pinniped ankle: A three-dimensional quantitative analysis of carnivoran tarsal evolution. In E. J. Sargis & M. Dagosto (Eds.), Mammalian evolutionary morphology (pp. 167–196). Netherlands: Springer.
Prideaux, G. J., & Warburton, N. M. (2010). An osteology-based appraisal of the phylogeny and evolution of kangaroos and wallabies (Macropodidae: Marsupialia). Zoological Journal of the Linnean Society, 159(4), 954–987.
Raerinne, J. (2011). Generalizations and models in ecology: Lawlikeness, invariance, stability, and robustness. https://helda.helsinki.fi/handle/10138/24583.
Rohlf, F. J. (2006). A comment on phylogenetic correction. Evolution, 60(7), 1509–1515.
Rohlf, F. J. (2009). NTSYSpc: Numerical taxonomy system, ver. 2.21r, Exeter Software. Setauket, New York: Exeter Publishing, Ltd.
Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39(1), 40–59.
Singleton, M. (2005). Functional shape variation in the cercopithecine masticatory complex. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 319–348). New York: Springer.
Weisbecker, V., & Goswami, A. (2010). Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proceedings of the National Academy of Sciences, 107(37), 16216–16221.
Wilson, D. E., & Reeder, D. M. (2005). Mammal species of the world: A taxonomic and geographic reference. Baltimore, MD: Johns Hopkins University Press.
Acknowledgments
We thank Robert Meredith (University of California, Riverside) for kindly helping us with the phylogenetic background, including the nexus file used to do the comparative analyses. Curators and collection managers at museums throughout Australia allowed access to their collections. AC is grateful to Krish Seetah (Stanford University), the Lang Fellowship and the Departments of Archaeology and Anthropology of Stanford University, for providing the stimulating academic environment in which this study was finalized, and to SYNTHESYS, an EC-funded Project for an integrated European infrastructure for natural history collections, for supporting both the previous study on CREA in placentals and its follow up in 2015. Many thanks also to Dean Adams (Indiana University), Emma Sherratt (University of New England) and Mark Collyer (Western Kentucky University) for their help with Geomorph and the interpretation of the differences in the phylogenetic regressions using MorphoJ and Geomorph. Finally, we are also in debt to the Editor-in-Chief and an anonymous reviewer for suggesting to better address the issues of sexual dimorphism and sampling error: thanks to their input, we added several analyses, which greatly improved the quality of the study and helped to strengthen its main conclusions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cardini, A., Polly, D., Dawson, R. et al. Why the Long Face? Kangaroos and Wallabies Follow the Same ‘Rule’ of Cranial Evolutionary Allometry (CREA) as Placentals. Evol Biol 42, 169–176 (2015). https://doi.org/10.1007/s11692-015-9308-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-015-9308-9