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.2016 Aug 24;13(1):39.
doi: 10.1186/s12983-016-0171-z. eCollection 2016.

Resolving the evolution of the mammalian middle ear using Bayesian inference

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Resolving the evolution of the mammalian middle ear using Bayesian inference

Héctor E Ramírez-Chaves et al. Front Zool..

Abstract

Background: 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. 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.

Results: Our 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.

Conclusions: Our 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.

Keywords: Australosphenida; Meckel’s groove; Middle ear detachment; Postdentary trough; Theria.

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Figures

Fig. 1
Fig. 1
Dentary ofa)Morganucodon with a mandibular middle ear based on the presence of a postdentary trough (redrawn from [48]);b Dentary ofLiaoconodon with a partial mammalian middle ear based on the presence of Meckel’s groove (redrawn from [9];c–e Dentary of the woylie,Bettongia penicillata at different developmental stages. c) presence of Meckel’s groove;d Meckel’s groove filled with the Meckel’s cartilage connecting the malleus to the dentary – this stage recapitulates or is similar to the partial mammalian middle ear found in some Cenozoic mammals;e individual showing a closed Meckel’s groove and absence of the connection, and hence, representing the definitive mammalian middle ear. The postdentary trough is not recapitulated during development in extant mammals. Orange, malleus; green, ectotympanic; blue, Meckel’s cartilage; light blue, incus; red, stapes; light green, incisor. Scale bar: 1 mm
Fig. 2
Fig. 2
A summary of parsimony inference for postdentary trough transformation based on four recent phylogenies [–24] with varying character coding. The reconstructions minimize the number of postdentary trough losses (blue) and regains (red). Note that taxon sampling differs between the studies (a-d). Placements of monotreme and therian mammals are represented by the platypus and ocelot, respectively. In Krause et al. [23] the symbols I and II indicate independent origins for australosphenidian taxa
Fig. 3
Fig. 3
Lingual view of the developing and artificially eroded platypus dentary. In early development of the platypus (a) Meckel’s cartilage lies in a deep Meckel’s groove. In a juvenile specimen with Meckel’s groove closed (b), a faint seam on the ventral border of the mandibular canal is present along the length of the dentary. Through relatively minor virtual erosion of the specimen (c–e), this trace is exaggerated into a structure resembling a Meckel’s groove while the detailed topology of the dentary is otherwise retained. Coding Meckel’s groove as present only where it is unambiguously well-developed (see Methods) therefore appears to be the best strategy
Fig. 4
Fig. 4
Bayesian inference of the loss of the postdentary trough among mammals (blue), based on the re-coded datasets (a–d [22];e–f [21]). Each tree summarizes the following analyses:a,b Shuotheriidae unconstrained (allowed to group with australosphenidans);b constraining monophyly of the multicuspate haramiyidans and multituberculates;c constraining Shuotheriidae to fall outside Mammalia;d excluding cheek teeth characters;e forcingKuehneotherium outside Mammalia;f allowingKuehneotherium to fall freely in the phylogeny. Postdentary trough is lost twice in all the analyses except in (b) when the earliest haramiyidans (e.gHaramiyavia) are forced together with Euharamiyida and multituberculates. The analyses excluding cheek teeth characters (d) place primitive haramiyidans outside Mammalia, with euharamiyidans and multituberculates both falling on the therian stem lineage–negating any requirement for a third loss of the postdentary trough in mammals. In (d)Haramiyavia is not included but likely forms a clade withMegaconus as observed in several of these trees (not b)
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