The bones of the vertebrate skull come from two developmental sources: the mesoderm and the neural crest. This dual origin allows to investigate how developmental properties influence evolutionary trends. In our paper published in Evolution Letters, we (Quentin, Tobias, Nathalie and international coauthors*) used comparative morphology to test whether the mesoderm- and the neural crest-derived bones show different evolutionary trends in lacertid lizards. First, we focused on the Common wall lizard, Podarcis muralis. The ‘nigriventris syndrome’ in P. muralis from Central Italy has been well studied by our team (e.g., Feiner et al., 2024, Science Advances). This syndrome consists of exaggerated traits involving exaggerated coloration, larger body size, more massive heads and aggressive behaviour, and has evolved by sexual selection (While et al., 2015, Ecology Letters). Since the neural crest cells are suspected to be involved in the making of the nigriventris syndrome, we expected the lizards with the nigriventris phenotype to differ from their ancestral conspecifics in the regions of the skull that are primarily derived from this cell type.
To successfully conduct these investigations, we used the extensive museum collections available at Museum Koenig Bonn and Hamburg and the Natural History Museum in Berlin. By using the imaging facilities of the Leibniz Institute for the Analysis of Biodiversity Changes and the Microscopy Facility of Department of Biology in Lund University, we produced high-resolution reconstructions (micro-CT scans) of P. muralis skulls that we compared with 3D morphometric analyses. Lizards with the nigriventris syndrome indeed showed elongated skulls, and the bones involved in this shape change were primarily derived from neural crest cells.
Together with our previous work, this clearly shows that sexual selection has caused the nigriventris lizards to diverge from their ancestral counterparts, and that the differences are most pronounced on neural crest-derived elements. But can the developmental biases resulting from the neural crest cells biology set evolutionary trends at larger scales? And what would these even look like? For the second phase of the project we broadened our investigations to lacertids, the family to which P. muralis belongs. Lacertids include 387 described species distributed across Eurasia and Africa, and their skull shape diversity has been linked to adaptations to diverse habitats and lifestyles (Hipsley & Müller, 2017, Evolution). We produced micro-CT scans of the skulls of 174 species and major lineages of lacertids to conduct comparative morphometric and phylogenetic analyses. We find that the dimension of morphological variation related to the nigriventris syndrome in P. muralis accounted for a significant proportion of the variation observed across lacertids. This indicates that diversification in lacertids is biased along the changes in skull shape associated with the nigriventris syndrome, most likely because of the conserved effects of the neural crest cells on development. Furthermore, neural crest derived bones were covarying (i.e., constituting modules) both within P. muralis and across lacertids. However, this neural crest-derived module appeared to be less evolvable (showed slower evolutionary rates and lower variance) than the module composed of mesoderm-derived bones. This discrepancy between the patterns observed at the micro- (the nigriventris syndrome) and the macroevolutionary scales (the lacertid family) may reflects developmental bias imposed by neural crest cell biology – yet playing out differently at different scales! By enabling developmental coupling of skull shape, body colouration and behaviour, the neural crest cells can facilitate rapid, correlated responses under sexual selection but may limit long-term evolvability in the skull.
*This work was conducted together with our collaborators Johannes Müller and Martin Kirchner (Museum für Naturkunde Berlin), Christy Hipsley (University of Copenhagen), Mariam Gabelaia, Juliane Vehof and Morris Flecks (Museum Koenig Bonn).