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Dynamic evolutionary interplay between ontogenetic skull patterning and whole-head integration

Nature Ecology & Evolution volume 8, pages 536–551 (2024)Cite this article

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Abstract

The arrangement and morphology of the vertebrate skull reflect functional and ecological demands, making it a highly adaptable structure. However, the fundamental developmental and macroevolutionary mechanisms leading to different vertebrate skull phenotypes remain unclear. Here we exploit the morphological diversity of squamate reptiles to assess the developmental and evolutionary patterns of skull variation and covariation in the whole head. Our geometric morphometric analysis of a complex squamate ontogenetic dataset (209 specimens, 169 embryos, 44 species), covering stages from craniofacial primordia to fully ossified bones, reveals that morphological differences between snake and lizard skulls arose gradually through changes in spatial relationships (heterotopy) followed by alterations in developmental timing or rate (heterochrony). Along with dynamic spatiotemporal changes in the integration pattern of skull bone shape and topology with surrounding brain tissues and sensory organs, we identify a relatively higher phenotypic integration of the developing snake head compared with lizards. The eye, nasal cavity and Jacobson’s organ are pivotal in skull morphogenesis, highlighting the importance of sensory rearrangements in snake evolution. Furthermore, our findings demonstrate the importance of early embryonic, ontogenetic and tissue interactions in shaping craniofacial evolution and ecological diversification in squamates, with implications for the nature of cranio-cerebral relations across vertebrates.

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Fig. 1: Squamate phylogeny and ontogenetic skull shape diversity.
Fig. 2: Patterns of diversification in head soft tissues during snake and lizard ontogeny.
Fig. 3: Integration pattern of developing soft tissues and skull parts in snakes and lizards.
Fig. 4: Shape integration of skull bones with soft tissues in squamates.
Fig. 5: Head integration beyond shape parameters.
Fig. 6: Ontogenetic model of skull evolution and integration pattern.

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Data availability

Raw landmark data, encompassing all the required landmarks needed for replicating the analyses, and surface files used for visualization are available on the Zenodo repository (https://zenodo.org/record/8376575). CT-scan data for key adult squamate species and the embryonic series of L. lugubris are publicly available in the published literature53,88 and Morphosource database (https://www.morphosource.org/), respectively.

Code availability

R scripts for conducting the analyses and surface files used in specific analyses are available on the Zenodo repository (https://zenodo.org/record/8376575).

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Acknowledgements

We thank A.-C. Aho, M. Partanen, M. Snepere, T. Ahlskog and J. Ulpovaara for technical assistance in captive breeding and animal care; O. Ovaskainen and H. Laakkonen (Finnish Museum of Natural History) for specimen loans; Helsinki X-ray Laboratory, Department of Physics (University of Helsinki), and especially H. Suhonen and H. Help for access to X-ray CT facilities and assistance with scanning large samples; A. Griffing for providing access to Lepidodactylus lugubris CT data from www.MorphoSource.org (collection of the University of Florida, IP holder Marquette University, funded by National Science Foundation grants: Division of Environmental Biology, grant numbers 1657662 and 1657656, Division of Biological Infrastructure, grant number 1701714); J. Eymann and D. Razmadze for technical assistance; D. Esquerre for the code provided for the heterochrony analysis; K. Happonen for helpful assistance on the spline analysis; M. and P. Joki, Tropicario and LL Reptiles for the chameleon, python and corn snake eggs provided for this study; R. Johansson for a sample donation; K. Koponen, M. Launiainen, A. Seppälä, J. Jalkanen, T. Rissanen, M. Tiusanen, M. Aulio, P. Puustinen, M. P. Pulkkinen, J. Takkinen and L. Sagath for assistance in field work; all the landowners for the permits given for field work; members of the Di-Poï laboratory and R. Rice, L. Säilä-Corfe and J. Jernvall for helpful discussions; and D. Ho for proofreading. This work was supported by funds from the Academy of Finland (decision 321910 to N.D.-P.), Institute of Biotechnology (to N.D.-P.), Sigrid Jusélius Foundation (to N.D.-P.), Minerva Foundation (to N.D.-P.), Integrative Life Science Doctoral Program (to J.O.), Finnish Cultural Foundation (to J.O.), Kuopion Luonnon Ystävien Yhdistys (to J.O.), Societas Biologica Fennica Vanamo (to J.O.), Ella and Georg Ehrnrooth Foundation (to J.O.), Oskar Öflund Stiftelse sr (to J.O.), Doctoral School in Health Sciences (to J.O.), Swedish Cultural Foundation in Finland (to I.-M.A.), Carl Gans Foundation (to J.O.) and Deputyship for Research & lnnovation, Ministry of Education in Saudi Arabia (project number 445-5-702 to E.R.K.).

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Authors and Affiliations

  1. Institute of Biotechnology, Helsinki Institute of Life Science, University of Helsinki, Helsinki, Finland

    Joni Ollonen, Simone Macrì, Ida-Maria Aalto & Nicolas Di-Poï

  2. Biology Department, College of Science, Taibah University, Al Madinah Al Munawwarah, Saudi Arabia

    Eraqi R. Khannoon

  3. Zoology Department, Faculty of Science, Fayoum University, Fayoum, Egypt

    Eraqi R. Khannoon

  4. National Museum of Natural History, Bulgarian Academy of Sciences, Sofia, Bulgaria

    Vladislav Vergilov

  5. Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland

    Jaakko Kuurne, Jarmo Saarikivi & Arttu Soukainen

  6. Senckenberg Centre for Human Evolution and Palaeoenvironment, Eberhard Karls Universität, Tübingen, Germany

    Ingmar Werneburg

  7. Fachbereich Geowissenschaften, Eberhard Karls Universität, Tübingen, Germany

    Ingmar Werneburg

  8. Department of Biological Sciences, California State University, Los Angeles, CA, USA

    Raul E. Diaz Jr

  9. Department of Herpetology, Natural History Museum of Los Angeles County, Los Angeles, CA, USA

    Raul E. Diaz Jr

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  1. Joni Ollonen
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Contributions

J.O. and N.D.-P. designed and planned the overall experimental approach. J.O., E.R.K., S.M., V.V., J.K., J.S., A.S, I.W., R.E.D. and N.D.-P. contributed to embryonic and/or postnatal specimen collection and preparation. Micro-CT scans were carried out by J.O., S.M., J.K, A.S. and I.-M.A. The 3D reconstructions and segmentations were carried out by J.O. and S.M. J.O. collected the 3D landmark data and performed all geometric morphometric and statistical analyses. J.O. and N.D.-P. created the figures and wrote the article. All co-authors contributed in the form of discussion and critical comments. All authors approved the final version of the article.

Corresponding author

Correspondence to Nicolas Di-Poï.

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Extended data

Extended Data Fig. 1 Reconstruction of ancestral trajectories.

Ancestral trajectories of modern snake (black) and toxicoferans (light grey) for skull (a, c, e) and soft tissues (b, d, f) at stages 1–2 (a, b), stage 3 (c, d), and stages 4–5 (e, f). The reconstructions involved the estimation of the ancestral intercept, angle, as well as minimum and maximum size. The five main developmental stages (stages 1–5) are colour-coded as before. Species names and the nodes employed for the reconstructions are indicated on the phylogenetic trees. Silhouettes from PhyloPic.org (creator credits: snake, Michael Keesay; lizard, Jose Carlos Arenas-Monroy).

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Supplementary Information

Supplementary Figs. 1–34, Tables 1–87 and References.

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Ollonen, J., Khannoon, E.R., Macrì, S. et al. Dynamic evolutionary interplay between ontogenetic skull patterning and whole-head integration. Nat Ecol Evol 8, 536–551 (2024). https://doi.org/10.1038/s41559-023-02295-3

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