Mammalian development does not recapitulate suspected key transformations in the evolution of the mammalian middle ear

Abstract

The tympanic ring, malleus and incus of the mammalian middle ear derive from the ancestral primary jaw joint of land vertebrates. In Mesozoic mammals, evolutionary detachment of the mammalian middle ear from the lower jaw occurred when Meckels cartilage - the last connection between the middle ear bones and the dentary - disappeared. This disappearance is famously recapitulated in early mammalian development. By extension, it was suggested that other developmental processes also recapitulate specific evolutionary processes that led to mammalian middle ear detachment in Mesozoic mammals. Specifically, developmental posterior/medial displacement and negative allometry of the growing ear ossicles relative to the lower jaw are thought to reflect evolutionary triggers of mammalian middle ear detachment. However, these hypotheses rest on scant developmental data, and have not been tested in a quantitative framework. Here we show, based on CT scans of developmental series of several marsupials and monotremes, that negative allometry of mammalian middle ear bones relative to the skull occurs only after mammalian middle ear detachment, ruling it out as a developmental detachment trigger. There is also no positional change of ectotympanic or malleus relative to the dentary. The mammalian middle ear bones are differently positioned in two monotreme species, a recent change which is not developmentally recapitulated. Together, our results challenge the developmental prerequisites of previously proposed evolutionary detachment processes, arguing specifically against causal links between mammalian middle ear detachment and brain expansion. Our data are more consistent with a biomechanical detachment trigger relating to the onset of dentary function, but more biomechanical work and palaeontological data are required to test this notion.