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The skull roof tracks the brain during the evolution and development of reptiles including birds

Nature Ecology & Evolution volume 1, pages 1543–1550 (2017)Cite this article

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Abstract

Major transformations in brain size and proportions, such as the enlargement of the brain during the evolution of birds, are accompanied by profound modifications to the skull roof. However, the hypothesis of concerted evolution of shape between brain and skull roof over major phylogenetic transitions, and in particular of an ontogenetic relationship between specific regions of the brain and the skull roof, has never been formally tested. We performed 3D morphometric analyses to examine the deep history of brain and skull-roof morphology in Reptilia, focusing on changes during the well-documented transition from early reptiles through archosauromorphs, including nonavian dinosaurs, to birds. Non-avialan taxa cluster tightly together in morphospace, whereas Archaeopteryx and crown birds occupy a separate region. There is a one-to-one correspondence between the forebrain and frontal bone and the midbrain and parietal bone. Furthermore, the position of the forebrain–midbrain boundary correlates significantly with the position of the frontoparietal suture across the phylogenetic breadth of Reptilia and during the ontogeny of individual taxa. Conservation of position and identity in the skull roof is apparent, and there is no support for previous hypotheses that the avian parietal is a transformed postparietal. The correlation and apparent developmental link between regions of the brain and bony skull elements are likely to be ancestral to Tetrapoda and may be fundamental to all of Osteichthyes, coeval with the origin of the dermatocranium.

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Fig. 1: Summary of skull roof evolution and relationship to soft tissue structures in Reptilia.
Fig. 2: Oblique dorsolateral views of skull roofs, braincases and brain endocasts of selected newly sampled fossil taxa, anterior to the lower left.
Fig. 3: 3D geometric morphometric principal component analyses (PCAs) of brains and skull roofs in reptiles.
Fig. 4: Relationship between the positions of the frontoparietal suture and forebrain–midbrain boundary.
Fig. 5: Ossification of cranial elements in embryonic alligator and chicken.
Fig. 6: Ossification of the frontal and parietal bones in embryonic alligator, chicken and lizard.

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References

  1. Richtsmeier, J. T. & Flaherty, K. Hand in glove: brain and skull development and dysmorphogenesis. Acta Neuropathol. 125, 469–489 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Richtsmeier, J. T. et al. Phenotypic integration of neurocranium and brain. J. Exper. Zool 306, 360–378 (2006).

    Article  Google Scholar 

  3. Koyabu, D. et al. Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size. Nat. Commun. 5, 3625 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Rowe, T. in Evolution of Nervous Systems Vol. 2 (ed. Kaas, J. H.) 1–52 (Elsevier, 2017).

  5. Jiang, X., Iseki, S., Maxon, R. E., Sucov, H. M. & Morriss-Kay, G. M. Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241, 106–116 (2002).

    Article  CAS  PubMed  Google Scholar 

  6. Morriss-Kay, G. M. Derivation of the mammalian skull vault. J. Anat. 199, 143–151 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Noden, D. M. Interactions and fates of avian craniofacial mesenchyme. Development 103, 121–140 (1988).

    PubMed  Google Scholar 

  8. Marcucio, R. S., Young, N. M., Hu, D. & Hallgrimsson, B. Mechanisms that underlie co-variation of the brain and face. Genesis 49, 177–189 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Marcucio, R. S., Cordero, D. R., Hu, D. & Helms, J. A. Molecular interactions coordinating the development of the forebrain and face. Dev. Biol. 284, 48–61 (2005).

    Article  CAS  PubMed  Google Scholar 

  10. Hu, D. & Marcucio, R. S. A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136, 107–116 (2009).

    Article  CAS  PubMed  Google Scholar 

  11. Bhullar, B. A. S. et al. A molecular mechanism for the origin of a key evolutionary innovation, the bird beak and palate, revealed by an integrative approach to major transitions in vertebrate history. Evolution 69, 1665–1677 (2015).

    Article  PubMed  Google Scholar 

  12. Abzhanov, A., Protas, M., Grant, B. R., Grant, P. R. & Tabin, C. J. Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305, 1462–1465 (2004).

    Article  CAS  PubMed  Google Scholar 

  13. Balanoff, A. M., Bever, G. S., Rowe, T. B. & Norell, M. A. Evolutionary origins of the avian brain. Nature 501, 93–96 (2013).

    Article  CAS  PubMed  Google Scholar 

  14. Hopson, J. A. Relative brain size and behavior in archosaurian reptiles. Ann. Rev. Ec. System. 8, 429–448 (1977).

    Article  Google Scholar 

  15. Marugán-Lobón, J., Watanabe, A. & Kawabe, S. Studying avian encephalization with geometric morphometrics. J. Anat. 229, 191–203 (2016).

    Article  PubMed  Google Scholar 

  16. Couly, G. F., Coltey, P. M. & Le Douarin, N. M. The triple origin of skull in higher vertebrates: a study in the quail-chick chimeras. Development 117, 409–429 (1993).

    CAS  PubMed  Google Scholar 

  17. Maddin, H. C., Piekarski, N., Sefton, E. M. & Hanken, J. Homology of the cranial vault in birds: new insights based on embryonic fate-mapping and character analysis. R. Soc. Open Sci. 3, 160356 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Noden, D. M. & Trainor, P. A. Relations and interactions between cranial mesoderm and neural crest populations. J. Anat. 207, 575–601 (2005).

    PubMed  PubMed Central  Google Scholar 

  19. Pinna, M. C. Concepts and tests of homology in the cladistic paradigm. Cladistics 7, 367–394 (1991).

    Article  Google Scholar 

  20. Bhullar, B. A. S. et al. How to make a bird skull: Major transitions in the evolution of the avian cranium, paedomorphosis, and the beak as a surrogate hand. Integ. Comp. Biol. 56, 389–403 (2016).

  21. Bhullar, B. A. S. et al. Birds have paedomorphic dinosaur skulls. Nature 487, 223–226 (2012).

    Article  CAS  PubMed  Google Scholar 

  22. Gauthier, J., Estes, R. & de Queiroz, K. in Phylogenetic Relationships of the Lizard Families: Essays Commemorating Charles L. Camp (eds Estes, R. & Pregill, G.) 15–98 (Stanford Univ. Press, 1988).

  23. Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Museum Nat. Hist. 352, 1–292 (2011).

    Article  Google Scholar 

  24. Butler, R., Sullivan, C. & Ezcurra, M. New clade of enigmatic early archosaurs yields insights into early pseudosuchian phylogeny and the biogeography of the archosaur radiation. BMC Evol. Biol. 14, 128 (2014).

    Google Scholar 

  25. Abzhanov, A., Rodda, S. J., McMahon, A. P. & Tabin, C. J. Regulation of skeletogenic differentiation in cranial dermal bone. Development 134, 3133–3144 (2007).

    Article  CAS  PubMed  Google Scholar 

  26. Gross, J. B. & Hanken, J. Review of fate-mapping studies of osteogenic cranial neural crest in vertebrates. Dev. Biol. 317, 389–400 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Chai, Y., Jiang, X., Ito, Y., Bringas, P. & Han, J. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671–1679 (2000).

    CAS  PubMed  Google Scholar 

  28. Kague, E. et al. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS One 7, e47394 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Clark, C. & Smith, K. Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J. Morphol. 215, 119–149 (1993).

    Article  CAS  PubMed  Google Scholar 

  30. De Beer, G. R. The Development of the Vertebrate Skull (Clarendon, 1937)

  31. Cuff, A. R. & Rayfield, E. J. Retrodeformation and muscular reconstruction of ornithomimosaurian dinosaur crania. PeerJ 3, e1093 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Dryden, I. L. & Mardia, K. V. Statistical Shape Analysis (Wiley, 1998).

  33. Rohlf, F. J. Shape statistics: procrustes superimpositions and tangent spaces. J. Classif. 16, 197–223 (1999).

    Article  Google Scholar 

  34. Klinberger, C. P. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11, 353–357 (2011).

    Article  Google Scholar 

  35. Hartigan, J. A. & Wong, M. A. Algorithm AS 136: a k-means clustering algorithm. J. R. Statist. Soc. Ser. C 28, 100–108 (1979).

    Google Scholar 

  36. Charrad, M., Ghazzali, N., Boiteau, V., Niknafs, A. & Charrad, M. M. Package ‘NbClust’. J. Stat. Softw. 61, 1–36 (2014).

    Article  Google Scholar 

  37. Adams, D. C. & Otárola-Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).

    Article  Google Scholar 

  38. Adams, D. C. & Collyer, M. L. Permutation tests for phylogenetic comparative analyses of high-dimensional shape data: what you shuffle matters. Evolution 69, 823–829 (2015).

    Article  PubMed  Google Scholar 

  39. Adams, D. C. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7, 565–572 (2016).

    Article  Google Scholar 

  40. Klingenberg, C. P. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol. Dev. 11, 405–421 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Klingenberg, C. P. Morphological integration and developmental modularity. Annu. Rev. Ecol. Evol. System. 39, 115–132 (2008).

    Article  Google Scholar 

  42. Rohlf, F. J. The tps series of software. Hystrix 26, 9–12 (2015).

    Google Scholar 

  43. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis v.3.04 (2015); http://mesquiteproject.org.

  44. Pinheiro, F. L., França, M. A., Lacerda, M. B., Butler, R. J. & Schultz, C. L. An exceptional fossil skull from South America and the origins of the archosauriform radiation. Sci. Rep. 6, 22817 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Gauthier, J. A., Kearney, M., Maisano, J. A., Rieppel, O. & Behlke, A. D. Assembling the squamate tree of life: perspectives from the phenotype and the fossil record. Bull. Peabody Museum Nat. Hist. 53, 3–308 (2012).

    Article  Google Scholar 

  46. Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Museum Nat. Hist. 352, 1–292 (2011).

    Article  Google Scholar 

  47. Carrano, M. T., Benson, R. B. & Sampson, S. D. The phylogeny of Tetanurae (Dinosauria: Theropoda). J. System. Palaeontol. 10, 211–300 (2012).

    Article  Google Scholar 

  48. Brusatte, S. L., Lloyd, G. T., Wang, S. C. & Norell, M. A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition. Curr. Biol. 24, 2386–2392 (2014).

    Article  CAS  PubMed  Google Scholar 

  49. Prum, R. O. et al. Comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).

    Article  CAS  PubMed  Google Scholar 

  50. Brusatte, S. L. in Computational Paleontology (ed. Elawa, A. M. T.) 53–74 (Springer, 2011).

  51. Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).

    Article  Google Scholar 

  52. Shedlock, A. M. & Edwards, S. V. in The Timetree of Life (eds Hedges, S. B. & Kumar, S.) 375–379 (Oxford University Press, 2009).

  53. Orme, D. et al. The caper package: comparative analysis of phylogenetics and evolution in R v.0.5. (2013); http://cran.r-project.org/web/packages/caper/index.html.

  54. Lavin, S. R., Karasov, W. H., Ives, A. R., Middleton, K. M. & Garland, T. Jr Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Physiol. Biochem. Zool. 81, 526–550 (2008).

    Article  PubMed  Google Scholar 

  55. Gartner, G. E. et al. Phylogeny, ecology, and heart position in snakes. Physiol. Biochem. Zool. 83, 43–54 (2009).

    Article  Google Scholar 

  56. Diaz-Uriarte, R. & Garland, T. Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. System. Biol. 45, 27–47 (1996).

    Article  Google Scholar 

  57. Pagel, M. Inferring evolutionary processes from phylogenies. Zool. Scripta 26, 331–348 (1997).

    Article  Google Scholar 

  58. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).

    Article  CAS  PubMed  Google Scholar 

  59. Revell, L. J. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319–329 (2010).

    Article  Google Scholar 

  60. Blomberg, S. P., Garland, T. Jr & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    Article  PubMed  Google Scholar 

  61. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

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Acknowledgements

We are grateful to E. J. Rayfield, A. R. Cuff, Y. Kobayashi, S. Chatterjee, A. Turner and L. Witmer for providing CT data; to G. Watkins-Colwell for assisting with cleared and stained squamate embryo specimens; and to D. Smith for imaging. F. A. Jenkins, Jr, J. A. Gauthier, G. Wagner and G. Navalon provided useful discussion. E. M. Sefton, H. Maddin and J. Hanken commented on the early stages of the work as it was underway. All Yale authors are supported by funds from Yale University. D.J.F. is supported in part by NSF DDIG DEB 1500798 to B.-A.S.B and D.J.F. A.P. is supported by an NSF Postdoctoral Research Fellowship in Biology. J.C. was partially funded by an NSF Graduate Research Fellowship and by NSF DDIG DEB 1501690. A.A. was supported by NSF grant 1257122, the Templeton Foundation grant RFP-12-0 and by funds from Imperial College London. G.S.B, A.M.B., and M.A.N. are supported in part by NSF DEB 1457181.

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Author notes

  1. Eva Hoffman

    Present address: Jackson School of Geosciences and Vertebrate Paleontology Laboratory, The University of Texas at Austin, Austin, TX, 78705, USA

Authors and Affiliations

  1. Department of Geology and Geophysics and Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA

    Matteo Fabbri, Nicolás Mongiardino Koch, Adam C. Pritchard, Michael Hanson, Eva Hoffman, Daniel J. Field & Bhart-Anjan S. Bhullar

  2. Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    Gabriel S. Bever & Amy M. Balanoff

  3. Department of Organismal and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA

    Zachary S. Morris & Jasmin Camacho

  4. Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath, BA2 7AY, UK

    Daniel J. Field

  5. Macaulay Curator, Division of Paleontology, American Museum of Natural History, New York, NY, 10024, USA

    Mark A. Norell

  6. Natural History Department, Iziko South African Museum, Cape Town, 8000, South Africa

    Roger M. Smith

  7. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK

    Arhat Abzhanov

  8. Natural History Museum, London, SW7 5BD, UK

    Arhat Abzhanov

  9. Jackson School of Geosciences and Vertebrate Paleontology Laboratory, The University of Texas at Austin, Austin, TX, 78705, USA

    Timothy B. Rowe

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Contributions

B-A.S.B. and A.A. conceived and planned the research. M.F., A.C.P., M.H., E.H., G.S.B., A.M.B., J.C., Z.M., D.J.F. and B.-A.S.B. scanned specimens and performed segmentation. M.F., N.M.K., A.C.P., M.H., and B.-A.S.B. placed landmarks and performed morphometric analyses. M.F. and N.M.K. performed correlation tests. M.F., N.M.K., A.C.P., M.H., E.H., G.S.B., T.B.R., A.A., and B.-A.S.B., wrote the paper. M.A.N. and R.M.S. provided CT data and assisted in anatomical interpretation.

Corresponding authors

Correspondence to Matteo Fabbri, Arhat Abzhanov or Bhart-Anjan S. Bhullar.

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Supplementary Figures 1–5, Supplementary Tables 1–3

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Landmark data for geometric morphometrics

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Fabbri, M., Mongiardino Koch, N., Pritchard, A.C. et al. The skull roof tracks the brain during the evolution and development of reptiles including birds. Nat Ecol Evol 1, 1543–1550 (2017). https://doi.org/10.1038/s41559-017-0288-2

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