Abstract
BackgroundThe minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint. This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. Recent parsimony analyses of modern and fossil mammals imply up to seven independent postdentary trough losses or even reversals, which is unexpected given the complexity of these transformations. Here we employ the first model-based, probabilistic analysis of the evolution of the definitive mammalian middle ear, supported by virtual 3D erosion simulations to assess for potential fossil preservation artifacts.ResultsOur results support a simple, biologically plausible scenario without reversals. The middle ear bones detach from the postdentary trough only twice among mammals, once each in the ancestors of therians and monotremes. Disappearance of Meckel’s cartilage occurred independently in numerous lineages from the Late Jurassic to the Late Cretaceous. This final separation is recapitulated during early development of extant mammals, while the earlier-occurring disappearance of a postdentary trough is not.ConclusionsOur results therefore suggest a developmentally congruent and directional two-step scenario, in which the parallel uncoupling of the auditory and feeding systems in northern and southern hemisphere mammals underpinned further specialization in both lineages. Until ~168 Ma, all known mammals retained attached middle ear bones, yet all groups that diversified from ~163 Ma onwards had lost the postdentary trough, emphasizing the adaptive significance of this transformation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0171-z) contains supplementary material, which is available to authorized users.
Highlights
The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint
A detached middle ear has been considered a defining feature of living mammals [10, 11], there is mounting evidence that the definitive mammalian middle ear (DMME) was acquired independently in monotremes and therians [7, 10, 12,13,14,15], which suggests strong selection for a sensitive auditory system adapted to high-frequency sounds [16, 17]
The most plesiomorphic is the mandibular middle ear of cynodonts (MMEC; Fig. 1a), in which the middle ear bones are fully attached to the posterior part of the dentary, and are housed in a postdentary trough and angular fossa
Summary
The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. One of the most famous and complicated transformations in vertebrate evolution is the origin of the mammalian middle ear bones (ectotympanic, incus and malleus) from load-bearing post-dentary elements (angular, articular and quadrate) during the evolution of synapsids [1]. This is the oldest and best-documented example of developmental recapitulation of an evolutionary transformation [2,3,4,5], as the final separation of the middle ear from the dentary through disappearance of Meckel’s. The PMME is found in early stages of middle ear development in extant mammals (Fig. 1c), reinforcing the impression that it represents an intermediate evolutionary condition [6]
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