Evolutionary Biology

, Volume 44, Issue 4, pp 476–495 | Cite as

Anyone with a Long-Face? Craniofacial Evolutionary Allometry (CREA) in a Family of Short-Faced Mammals, the Felidae

  • Davide Tamagnini
  • Carlo Meloro
  • Andrea Cardini
Research Article


Among adults of closely related species, a trend in craniofacial evolutionary allometry (CREA) for larger taxa to be long-faced and smaller ones to have paedomorphic aspects, such as proportionally smaller snouts and larger braincases, has been demonstrated in some mammals and two bird lineages. Nevertheless, whether this may represent a ‘rule’ with few exceptions is still an open question. In this context, Felidae is a particularly interesting family to study because, although its members are short-faced, previous research did suggest relative facial elongation in larger living representatives. Using geometric morphometrics, based on two sets of anatomical landmarks, and traditional morphometrics, for comparing relative lengths of the palate and basicranium, we performed a series of standard and comparative allometric regressions in the Felidae and its two subfamilies. All analyses consistently supported the CREA pattern, with only one minor exception in the geometric morphometric analysis of Pantherinae: the genus Neofelis. With its unusually long canines, Neofelis species seem to have a relatively narrow cranium and long face, despite being smaller than other big cats. In spite of this, overall, our findings strengthen the possibility that the CREA pattern might indeed be a ‘rule’ among mammals, raising questions on the processes behind it and suggesting future directions for its study.


Anatomical landmarks Comparative method Evolutionary rule Felinae Geometric morphometrics Pantherinae Regression Shape 



We are deeply grateful to all scientists and institutions who made pictures of crania freely available on their websites, and also to Mike Collyer and Dean Adams for help with geomorph, to Marko Djurakic for suggestions on R scripts, and to Jim Rohlf and Liam Revell for their advice on MA regressions. We are in debt also 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.

Supplementary material

11692_2017_9421_MOESM1_ESM.txt (20 kb)
Supplementary material 1 (TXT 20 KB)
11692_2017_9421_MOESM2_ESM.xls (34 kb)
Supplementary material 2 (XLS 34 KB)


  1. Adams, D. C., Cardini, A., Monteiro, L. R., O’Higgins, P., & Rohlf, F. J. (2011). Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters. Journal of human evolution, 60, 240–243.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. Adams, D. C., & Collyer, M. L. (2015). Permutation tests for phylogenetic comparative analyses of high-dimensional shape data: What you shuffle matters. Evolution, 69, 823–829.CrossRefPubMedGoogle Scholar
  4. Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.CrossRefGoogle Scholar
  5. 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, 7–14.Google Scholar
  6. Adams, D. C., Collyer, M., Kaliontzopoulu, A., & Sherratt, E. (2016). Geomorph: Geometric morphometric analysis of 2D/3D landmark data. Version 3.0.3, Retrieved
  7. Agnarsson, I., Kuntner, M., & May-Collado, L. J. (2010). Dogs, cats, and kin: A molecular species-level phylogeny of Carnivora. Molecular Phylogenetics and Evolution, 54, 726–745.CrossRefPubMedGoogle Scholar
  8. Arnold, C., Matthews L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Evolutionary Anthropology: Issues, News, and Reviews 19, 114–118.CrossRefGoogle Scholar
  9. Boettiger, C., Coop, G., & Ralph, P. (2012). Is your phylogeny informative? measuring the power of comparative methods. Evolution, 66, 2240–2251.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bright, J. A., Marugán-Lobón, J., Cobb, S. N., et al. (2016). The shapes of bird beaks are highly controlled by nondietary factors. Proceedings of the National Academy of Sciences, 113, 5352–5357.CrossRefGoogle Scholar
  11. Carbone, C., Mace, G. M., Roberts, S. C., & Macdonald, D. W. (1999). Energetic constraints on the diet of terrestrial carnivores. Nature, 402, 286–288.CrossRefPubMedGoogle Scholar
  12. Cardini, A. (2014). Missing the third dimension in geometric morphometrics: How to assess if 2D images really are a good proxy for 3D structures? Hystrix, The Italian Journal of Mammalogy, 25, 73–81.Google Scholar
  13. Cardini, A. (2017). Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. Journal of Zoological Systematics and Evolutionary Research, 55, 1–10.CrossRefGoogle Scholar
  14. Cardini, A., & Elton, S. (2007). Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology, 126, 121–134.CrossRefGoogle Scholar
  15. Cardini, A., & Polly, P. D. (2013). Larger mammals have longer faces because of size-related constraints on skull form. Nature Communications, 4, 2458.CrossRefPubMedGoogle Scholar
  16. Cardini, A., Polly, P. D., Dawson, R., & Milne, N. (2015a). Why the long face? Kangaroos and Wallabies follow the same ‘Rule’ of cranial evolutionary allometry (CREA) as placentals. Evolutionary Biology, 42, 169–176.CrossRefGoogle Scholar
  17. Cardini, A., Seetah, K., & Barker, G. (2015b). How many specimens do I need? Sampling error in geometric morphometrics, testing the sensitivity of means and variances in simple randomized selection experiments. Zoomorphology, 134, 149–163.CrossRefGoogle Scholar
  18. Cardini, A. (2013). Geometric morphometrics. In Encyclopedia of life support systems (EOLSS), Developed under the Auspices of the UNESCO, Eolss Publishers, Paris, Retrieved
  19. Cardini, A. (2016). Why the long face? Evidence for (or against?) a new ‘rule’ in mammalian evolution. 96th Annual Meeting of the American Society of Mammalogists, Abstract Book.Google Scholar
  20. 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
  21. Christiansen, P. (2008). Evolutionary convergence of primitive sabertooth craniomandibular morphology: the clouded leopard (Neofelis nebulosa) and Paramachairodus ogygia compared. Journal of Mammalian Evolution, 15, 155–179.CrossRefGoogle Scholar
  22. Clauss, M., Dittmann, M. T., Müller, D. W. H., Meloro, C., & Codron, D. (2013). Bergmann′s rule in mammals: A cross-species interspecific pattern. Oikos, 122, 1465–1472.Google Scholar
  23. Cooper, N., Thomas, G. H., Venditti, C., Meade, A., & Freckleton, R. P. (2016). A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biological Journal of the Linnean Society, 118, 64–77.CrossRefPubMedGoogle Scholar
  24. Drake, A. G., & Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. The American Naturalist, 175, 289–301.CrossRefPubMedGoogle Scholar
  25. Díaz-Uriarte, R., & Garland, T. (1998). Effects of branch length errors on the performance of phylogenetically independent contrasts. Systematic Biology, 47, 654–672.CrossRefPubMedGoogle Scholar
  26. Fruciano, C. (2016). Measurement error in geometric morphometrics. Development Genes and Evolution, 226, 139–158.CrossRefPubMedGoogle Scholar
  27. Garland, T., Midford, P. E., & Ives, A. R. (1999). An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Integrative and Comparative Biology, 39, 374–388.Google Scholar
  28. Hammer, O., Harper, D., & Ryan, P. (2001). PAST: Paleontological statistics software package for education and data analysis. Paleontologia Electron, 4(1), 1–9.Google Scholar
  29. Hartstone-Rose, A., Perry, J. M., & Morrow, C. J. (2012). Bite force estimation and the fiber architecture of felid masticatory muscles. The Anatomical Record, 295, 1336–1351.CrossRefPubMedGoogle Scholar
  30. Jhwueng, D. C. (2013). Assessing the goodness of fit of phylogenetic comparative methods: A meta-analysis and simulation study. PLoS ONE, 8, e67001.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Johnson, W. E., Eizirik, E., Pecon-Slattery, J., Murphy, W. J., Antunes, A., Teeling, E., & O’Brien, S. J. (2006). The late miocene radiation of modern Felidae: A genetic assessment. Science, 311, 73–77.CrossRefPubMedGoogle Scholar
  32. Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.CrossRefPubMedGoogle Scholar
  33. Klingenberg, C. P. (2013). Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix, The Italian Journal of Mammalogy, 24, 15–24.Google Scholar
  34. Klingenberg, C. P. (2016). Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226, 113–137.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56, 1909–1920.CrossRefPubMedGoogle Scholar
  36. 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, 591–610.CrossRefPubMedGoogle Scholar
  37. Linde-Medina, M. (2016). Testing the cranial evolutionary allometric ‘rule’ in Galliformes. Journal of Evolutionary Biology, 29, 1873–1878.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Marcus, L. F. (1990. Traditional morphometrics. In F. J. Rohlf & F. L. Bookstein (Eds.) Proceedings of the Michigan morphometrics workshop. (pp.77–122). Ann Arbor: University of Michigan Museum of ZoologyGoogle Scholar
  39. Meachen-Samuels, J., & Van Valkenburgh, B. (2009a). Craniodental indicators of prey size preference in the Felidae. Biological Journal of the Linnean Society, 96, 784–799.CrossRefGoogle Scholar
  40. Meachen-Samuels, J., & Van Valkenburgh, B. (2009b). Forelimb indicators of prey-size preference in the Felidae. Biological Journal of the Linnean Society, 96, 729–744.CrossRefGoogle Scholar
  41. Meloro, C., & O’Higgins, P. (2011). Ecological adaptations of mandibular form in fissiped Carnivora. Journal of Mammalian Evolution, 18, 185–200.CrossRefGoogle Scholar
  42. Meloro, C., & Slater, G. J. (2012). Covariation in the skull modules of cats: The challenge of growing saber-like canines. Journal of Vertebrate Paleontology, 32, 677–685.CrossRefGoogle Scholar
  43. Mitteroecker, P., Gunz, P., & Windhager, S., et al. (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
  44. Monteiro, L. (2013). Morphometrics and the comparative method: studying the evolution of biological shape. Hystrix, The Italian Journal of Mammalogy, 24, 25–32.Google Scholar
  45. Nowak, R. M. (2005). Walker’s carnivores of the world. Baltimore: JHU Press.Google Scholar
  46. Nowak, K., Cardini, A., & Elton, S. (2008). Evolutionary acceleration and divergence in Procolobus kirkii. International Journal of Primatology, 29, 1313.CrossRefGoogle Scholar
  47. Nowell, K. (2002). Revision of the Felidae red list of threatened species. Cat News, 37, 4–6.Google Scholar
  48. Nowell, K., Jackson, P., et al. (1996). Wild cats: status survey and conservation action plan. Gland: IUCN.Google Scholar
  49. Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England), 20, 289–290.CrossRefGoogle Scholar
  50. Pearson, A., Groves, C., & Cardini, A. (2015). The ‘temporal effect’ in hominids: Reinvestigating the nature of support for a chimp-human clade in bone morphology. Journal of Human Evolution, 88, 146–159.CrossRefPubMedGoogle Scholar
  51. Piras, P., Maiorino, L., Teresi, L., Meloro, C., Lucci, F., Kotsakis, T., & Raia, P. (2013). Bite of the cats: Relationships between functional integration and mechanical performance as revealed by mandible geometry. Systematic Biology, 62(6), 878–900.CrossRefPubMedGoogle Scholar
  52. R Core Team. (2016). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved
  53. Randau, M., Carbone, C., & Turvey, S. T. (2013). Canine evolution in sabretoothed carnivores: Natural selection or sexual selection? PLoS ONE, 8, e72868.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Rohlf, F. J. (2006). A comment on phylogenetic correction. Evolution, 60, 1509–1515.CrossRefPubMedGoogle Scholar
  55. Rohlf, F. J. (2015). The tps series of software. Hystrix, The Italian Journal of Mammalogy, 26, 9–12.Google Scholar
  56. Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39, 40–59.Google Scholar
  57. Sakamoto, M., & Ruta, M. (2012). Convergence and divergence in the evolution of cat skulls: Temporal and spatial patterns of morphological diversity. PLoS ONE, 7, e39752.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sanderson, J. G., & Watson, P. (2011). Small wild cats: The animal answer guide. Baltimore: JHU Press.Google Scholar
  59. Segura, V., Prevosti, F., & Cassini, G. (2013). Cranial ontogeny in the Puma lineage, Puma concolor, Herpailurus yagouaroundi, and Acinonyx jubatus (Carnivora: Felidae): A threedimensional geometric morphometric approach. Zoological Journal of the Linnean Society, 169, 235–250.CrossRefGoogle Scholar
  60. Segura, V., Cassini, G., & Prevosti, F. (2016). Three-dimensional cranial ontogeny in pantherines (P. leo, P. onca, P. pardus, P. tigris; Carnivora:, Felidae. Biological Journal of the Linnaean Society.Google Scholar
  61. Sicuro, F. L. (2011). Evolutionary trends on extant cat skull morphology (Carnivora: Felidae): A three-dimensional geometrical approach. Biological Journal of the Linnean Society, 103, 176–190.CrossRefGoogle Scholar
  62. Sicuro, F. L., & Oliveira, L. F. B. (2011). Skull morphology and functionality of extant Felidae (Mammalia: Carnivora): A phylogenetic and evolutionary perspective. Zoological Journal of the Linnean Society, 161, 414–462.CrossRefGoogle Scholar
  63. Sims, M. E. (2012). Cranial morphology of five felids: Acinonyx jubatus, Panthera onca, Panthera pardus, Puma concolor, Uncia uncia. Russian Journal of Theriology, 11, 157–170.CrossRefGoogle Scholar
  64. Slater, G. J., & Van Valkenburgh, B. (2008). Long in the tooth: Evolution of sabertooth cat cranial shape. Paleobiology, 34, 403–419.CrossRefGoogle Scholar
  65. Slater, G. J., & Van Valkenburgh, B. (2009). Allometry and performance: the evolution of skull form and function in felids. Journal of Evolutionary Biology, 22, 2278–2287.CrossRefPubMedGoogle Scholar
  66. Takahashi, H., Yamashita, M., & Shigehara, N. (2006). Cranial photographs of mammals on the web: the Mammalian Crania Photographic Archive (MCPA2) and a comparison of bone image databases. Anthropological Science, 114, 217–222.CrossRefGoogle Scholar
  67. Viscosi, V., & Cardini, A. (2011). Leaf morphology, taxonomy and geometric morphometrics: A simplified protocol for beginners. PLoS ONE, 6, e25630.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Warton, D. I., Duursma, R. A., Falster, D. S., et al. (2012). smatr 3—An R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3, 257–259.CrossRefGoogle Scholar
  69. Warton, D. I., Wright, I. J., Falster, D. S., et al. (2006). Bivariate line-fitting methods for allometry. Biological Reviews, 81, 259–291.CrossRefPubMedGoogle Scholar
  70. Werdelin, L. (1983). Morphological patterns in the skulls of cats. Biological Journal of the Linnean Society, 19, 375–391.CrossRefGoogle Scholar
  71. Werdelin, L., Yamaguchi, N., Johnson, W. E., et al. (2010). Phylogeny and evolution of cats (Felidae). Biology and conservation of wild felids. (pp. 59–82) Oxford: Oxford University Press.Google Scholar
  72. Wilson, D. E., & Reeder, D. M. (2005). Mammal species of the world: A taxonomic and geographic reference. Baltimore: JHU Press.Google Scholar
  73. Wilting, A., Christiansen, P., Kitchener, A. C., et al. (2011). Geographical variation in and evolutionary history of the Sunda clouded leopard (Neofelis diardi) (Mammalia: Carnivora: Felidae) with the description of a new subspecies from Borneo. Molecular Phylogenetics and Evolution, 58, 317–328.CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Dipartimento di Scienze Biologiche, Geologiche ed AmbientaliUniversità di BolognaBolognaItaly
  2. 2.Research Centre in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and PsychologyLiverpool John Moores UniversityLiverpoolUK
  3. 3.Dipartimento di Scienze Chimiche e GeologicheUniversità di Modena e Reggio EmiliaModenaItaly
  4. 4.School of Anatomy, Physiology and Human BiologyThe University of Western AustraliaCrawleyAustralia

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