Exploring ancestral phenotypes and evolutionary development of the mammalian middle ear based on Early Cretaceous Jehol mammals

Abstract

We report a new Cretaceous multituberculate mammal with 3D auditory bones preserved. Along with other fossil and extant mammals, the unequivocal auditory bones display features potentially representing ancestral phenotypes of the mammalian middle ear. These phenotypes show that the ectotympanic and the malleus-incus complex changed notably during their retreating from the dentary at various evolutionary stages and suggest convergent evolution of some features to extant mammals. In contrast, the incudomalleolar joint was conservative in having a braced hinge configuration, which narrows the morphological gap between the quadroarticular jaw joint of non-mammalian cynodonts and the incudomalleolar articulations of extant mammals. The saddle-shaped and abutting malleus-incus complexes in therians and monotremes, respectively, could have evolved from the braced hinge joint independently. The evolutionary changes recorded in the Mesozoic mammals are largely consistent with the middle ear morphogenesis during the ontogeny of extant mammal, supporting the relation between evolution and development.

Monotreme middle ear is not primitive for Mammalia

“…The authors hypothesized that a middle ear with a monotreme-like incus and malleus and incudomallear articulation was primitive for mammals, which challenges the convention that the monotreme middle ear is specialized 3 or autapomorphic 4 in mammals. We raise concerns about terminology and identification of the incus presented by Wang et al and show that their analysis does not support their hypothesis; instead, it supports the one by Mao et al 5,6 .…”

“…Contrary to the existing hypothesis that the braced hinge joint (=partial overlapping joint, POJ; Fig. 1b, i, j) is potentially primitive for mammals 6 , Wang et al concluded that optimization of five incudomallear characters in their phylogeny (Fig. 2a) ‘supports the overlapping joint as primitive for Mammalia.…”

“…The authors also thought that the incus ‘resembles’ and “has a similar outline” to those of the Jeholbaatar 13 and Arboroharamiya allinhopsoni 10–12 . However, the ‘incus’ of Jeholbaatar has been shown to be part of the malleus by new evidence 6 , as noted by Wang et al The only known unequivocal incus of euharamiyidans was from Arboroharamiya, a sister taxon of V. diplomylos , which has been repeatedly described as convex, bulbous, and like that of therians 10–12 . The ‘incus’ in Qishou (see ED fig.…”

“…Wang et al presented some valuable interpretations on previously known but still poorly understood auditory bones, such as the surangular and ectotympanic, in ‘haramiyidans’. Because these subjects have been extensively treated 2,5,6,10–12 , we focus our discussion on the incus and malleus that Wang et al provided some new evidence, which in turn led to their conclusion. The authors claimed that in their specimen (IMMNH-PV01699) the ossicular chain is ‘well-preserved and in near-life position’.…”

“… a , Mandibular middle ear of Morganucodon , showing the trochlear incudomallear joint. b , Diagram showing the braced hinge (partial overlapping) joint in cross-sectional view, which is based on i and j ; the incus is largely caudal to the malleus but laterally braced by a bony lip of the malleus 6 . c , Diagram showing the overlapping (abutting) joint in cross-sectional view, which is based on e and f ; the incus is dorsal to the malleus.…”