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

Abstract

The ectotympanic, malleus and incus of the developing mammalian middle ear (ME) are initially attached to the dentary via Meckel's cartilage, betraying their origins from the primary jaw joint of land vertebrates. This recapitulation has prompted mostly unquantified suggestions that several suspected-but similarly unquantified-key evolutionary transformations leading to the mammalian ME are recapitulated in development, through negative allometry and posterior/medial displacement of ME bones relative to the jaw joint. Here we show, using mCT reconstructions, that neither allometric nor topological change is quantifiable in the pre-detachment ME development of six marsupials and two monotremes. Also, differential ME positioning in the two monotreme species is not recapitulated. This challenges the developmental prerequisites of widely cited evolutionary scenarios of definitive mammalian middle ear (DMME) evolution, highlighting the requirement for further fossil evidence to test these hypotheses. Possible association between rear molar eruption, full ME ossification and ME detachment in marsupials suggests functional divergence between dentary and ME as a trigger for developmental, and possibly also evolutionary, ME detachment. The stable positioning of the dentary and ME supports suggestions that a 'partial mammalian middle ear' as found in many mammaliaforms-probably with a cartilaginous Meckel's cartilage-represents the only developmentally plausible evolutionary DMME precursor.

Resolving the evolution of the mammalian middle ear using Bayesian inference

“…This is also the oldest and best-documented example of developmental recapitulation of an evolutionary transformation [2–5], as the final separation of the middle ear from the dentary through disappearance of Meckel’s cartilage occurs in mammalian development as in evolution [6, 7] (Fig. 1).…”

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).…”

Prenatal allometric trajectories and the developmental basis of postcranial phenotypic diversity in bats (Chiroptera)

“…A limiting factor to our understanding of the evolution of postcranial adaptations for flight in bats (e.g., forelimb bone elongation, reduced cortical thickness, interdigital membranes) is the patchiness of the fossil record, which lacks postcranial transitional forms between the nonvolant bat ancestor and the oldest bat fossils known, and between modern bats with novel locomotory strategies and their most recent common ancestors (Eiting & Gunnell, ; Hand et al, , ). Further understanding of the developmental basis of flight adaptations in bats could inform understanding about the correspondence between the adaptations to selective pressures that taxa experience and fluctuations in their developmental trajectories (Geiger, Forasiepi, Koyabu & Sanchez‐Villagra ; Koyabu et al, ; Ramírez‐Chaves et al, ).…”