Resolving the evolution of the mammalian middle ear using Bayesian inference

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.

The vertebrate middle and inner ear: A short overview

“…Complex bone reorganization of the mandible occurred during detachment of the mammalian middle ear, which is well supported by fossil evidence (e.g., Allin & Hopson, 1992;Kermack, Mussett, & Rigney, 1981;Luo, Schultz, & Ekdale, 2016;Manley & Sienknecht, 2013;Martin & Luo, 2005;Meng, Bi, Zheng, & Wang, 2016;Meng, Wang, & Li, 2011). Clearing and staining techniques using ontogenetic sequences drew an even clearer picture of the evolution of the mammalian middle ear in more recent years (Anthwal et al, 2013;Ramírez-Chaves et al, 2016a;Ramírez-Chaves, Weisbecker, Wroe, & Phillips, 2016b;Rich, Hopson, Musser, Flannery, & Vickers-Rick, 2005;Urban et al, 2017).…”

Conflict Resolution for Mesozoic Mammals: Reconciling Phylogenetic Incongruence Among Anatomical Regions

“…However, some morphological character complexes may be expected to be less reliable. Molar cusp patterns, for instance, often possess a combination of rapid evolution (which erodes phylogenetic signal) and functional/developmental correlations that can overwhelm the remaining phylogenetic signal (Luo et al, 2001;Kangas et al, 2004;Ramírez-Chaves et al, 2016). However, non-phylogenetic sources of character covariation in vertebrate morphology are numerous and commonplace, including (but not limited to) allometry, pleiotropic-developmental, and functional correlations associated with ecological convergence or evolutionary trends (parallelism), and their respective influences vary dramatically across skeletal regions (Goswami et al, 2014;Cardini et al, 2015).…”

“…Five deeper-diverging cynodonts are used as outgroups to root the phylogeny. Within australosphenidans, coding changes were made on contentious mandibular characters related to the presence of a postdentary trough and Meckel's groove, following Ramírez-Chaves et al (2016). We also included the near-complete humerus from Kryoryctes, which provides the only stem monotreme postcranial information.…”

“…The trees were sampled every 5,000 generations, with the first 25% discarded as burn-in. Clade frequencies across the two independent runs reached convergence (average standard deviation of split frequencies < 0.01), and the estimated sample sizes for the tree prior, likelihood, and posterior estimates for tree lengths and rate alpha parameters were >200 (Tracer v1.7.1; Rambaut and Drummond, 2014).…”

“…These included the evolution of several character complexes that were upheld as high-value markers for defining mammalian taxonomic exclusion or inclusion but that have since been revealed to be homoplastic. For example, tribosphenic molars, which combine piercing/slicing and grinding functions, and detachment of the middle ear ossicles from the dentary have both now been shown to have evolved independently several times (Allin, 1975;Chow and Rich, 1982;Wang et al, 2001;Martin and Luo, 2005;Luo et al, 2007;Luo, 2011;Ramírez-Chaves et al, 2016).…”