Neural crest cell biology shapes lizard skull evolution across evolutionary time scales
Quentin J.B. Horta-LacuevaiD, Tobias UlleriD, Morris Flecks, Mariam GabelaiaiD, Christy A. HipsleyiD, Martin KirchneriD, Johannes MülleriD, Nathalie FeineriD
Abstract
The vertebrate skull originates from two embryonic lineages, the mesoderm and the neural crest, offering a unique framework to study how developmental mechanisms connect phenotypic variation and evolutionary diversification. Using 3D geometric morphometrics, we analysed skull shape variation in lacertid lizards. Mesoderm- and neural crest-derived bones formed distinct, conserved modules at both micro- and macroevolutionary scales. In the common wall lizard (Podarcis muralis), rapid evolution of skull shape under sexual selection was primarily driven by neural crest-derived bones. While the primary axis of shape divergence in P. muralis aligned with a major axis of variation across lacertids, neural crest-derived bones exhibited slower evolutionary rates and lower morphological disparity than mesodermal-derived bones. We propose that this discrepancy between the role of the neural crest for skull evolution on micro- and macroevolution reflects constraints imposed by neural crest cell biology: although developmental plasticity enables rapid, correlated responses under sexual selection, pleiotropy may limit long-term evolvability of neural crest-derived skull regions. Teaser textThe bones of the vertebrate skull come from two developmental sources: the mesoderm and the neural crest. This dual origin allows to study how development influences evolution. Using 3D models of lizard skulls--including a species with exaggerated male traits linked to the neural crest--we examined patterns of skull variation. We found that neural crest-derived bones contribute to rapid changes driven by sexual selection. However, across different species, these same skull regions evolve more slowly and show less variation. This suggests that while neural crest cells may constrain long-term evolution because of their wide influence, they can also enable fast adaptations. The developmental biology of a trait therefore shapes its evolution.
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