Shaping the mammalian skull
: Modelling how suture morphology, complexity, and development drive cranial evolution

    Student thesis: Doctoral ThesisDoctor of Philosophy

    Abstract

    Mammals exhibit an impressive amount of cranial phenotypic diversity, reflecting their extensive ecological diversity. Cranial morphology can provide us with an understanding of a species’ ecology, locomotion, and development, and thus has received considerable attention within morphometric studies. In stark contrast, little attention has been dedicated to the morphology of the sutural joints, between cranial bones, which are known to support an array of functions. Most notably, sutures provide active growth centres to facilitate cranial bone growth and thus their development is thought to be central in shaping the mammalian skull. However, the influence suture development has on cranial morphology has received even less study than the sutures themselves and has predominantly been focussed on developmental disorders such as craniosynostosis, rather than macroevolutionary patterns.

    In this thesis, I produce the largest three-dimensional morphometric dataset in an ontogenetic comparative framework to date, with 165 fetal to adult specimens representing 22 species that span the phylogenetic breadth of Mammalia. Using geometric morphometric techniques, I analyse patterns of morphological development for both the mammalian skull and cranial sutures and quantify the interaction between suture and skull development. Quantification of the interaction between suture and skull development will examine the hypothesis that variation in suture morphological development influences cranial phenotypic diversity across mammals.

    From the analyses of cranial morphological variation, I find that diverse mammal cranial phenotypes stem from diversity in their ontogenetic trajectories. Specifically, I observe a coneshaped pattern of cranial morphological development that is reflective of the upper half of the developmental hourglass model, indicating morphological divergence through ontogeny following the morphologically conserved fetal stage. For the first time within placental mammals, I find an association between the altricial-precocial spectrum and cranial morphology, highlighting an underappreciated role for the position along the altricial-precocial spectrum in shaping placental mammal skull morphological variation. I further identify interspecific variation in cranial ontogenetic trajectories and in particular a divergence between marsupial and placental cranial development.

    From the analyses of suture morphological variation, I find that suture fusion correlates with developmental age, suggesting that fusion may provide a reliable proxy for age for mammalian taxa. Given the highly distinct reproductive and developmental modes of marsupials and placentals, it was unsurprising to observe different patterns and rates of cranial suture fusion between the two infraclasses (marsupials and placentals). Most likely, differences in suture fusion pattern support the extended period of prolonged postnatal brain expansion evident in marsupials. Following a comparison of metrics used to determine suture complexity, I find that the complexity of the cranial sutures was greater for the sutures in contact with the underlying brain and for species with an extended period of postnatal brain growth (marsupials and the primate Sapajus apella). Collectively, suture morphological analyses suggest a relationship between postnatal brain growth and the developing sutures.

    In multiple chapters of this thesis I find, from both morphological analyses of cranial shape development and suture morphological development, clear differences in the pattern, timing, and rate of suture and skull development between marsupials and placentals, specifically localising these as paedomorphic shifts on the marsupial lineage. Contrary to previous hypotheses, I propose the novel hypothesis that placental mammal cranial and suture ontogeny better reflects the ancestral therian mammal, while the marsupial cranial and suture ontogenetic trajectories reflect the more derived state of mammal development. This finding reshapes our understanding of the evolution of mammalian cranial morphology. Moreover, it supports the previously proposed hypothesis that evolutionary innovations via heterochronic shifts do not necessarily facilitate morphological diversification but may also constrain morphological evolution, which is well reported for marsupials.

    Finally, through the incorporation of suture morphological data and skull morphological data, I provide empirical evidence for the relationship between suture morphology (fusion, shape, and complexity) and skull morphology. I find a highly integrated pattern of morphological development between the skull and cranial sutures and observe specific changes in cranial morphology in association with specific sutural changes. I propose that, as with craniosynostosis, developmental mechanisms shaping suture morphology are central to the evolution of mammalian cranial phenotypic diversity.

    This thesis represents a significant advance in the study of mammalian suture morphological development and evolution beyond model organisms, whilst enhancing our understanding of the developmental drivers behind the evolution of the mammalian skull. This work is unrivalled in its in-depth ontogenetic sampling and accompanying broad phylogenetic sampling across Mammalia and represents a step-change in our understanding of the central role sutures play in driving mammalian skull phenotypic diversity.




    Date of Award1 Aug 2022
    Original languageEnglish
    Awarding Institution
    • King's College London
    Supervisoraffiliated academic (Supervisor) & Abigail Tucker (Supervisor)

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