Inner ear labyrinth anatomy of monotremes and implications for mammalian inner ear evolution.

Abstract

The monophyletic clade Monotremata branches early from the rest of the mammalian crown group in the Jurassic and members of this clade retain many ancestral mammalian traits. Thus, accurate and detailed anatomical descriptions of this group can offer unique insight into the early evolutionary history of Mammalia. In this study, we examine the inner ear anatomy of two extant monotremes, Ornithorhynchus anatinus and Tachyglossus aculeatus, with the primary goals of elucidating the ancestral mammalian ear morphology and resolving inconsistencies found within previous descriptive literature. We use histological serial sections and high-resolution microcomputed tomography (µCT) for correlating soft tissue features of the vestibule and cochlea to the osseous labyrinth endocast. We found that in both monotremes the scala tympani coils to a lesser degree than scala vestibuli and scala media, although all three scalae show an apical coil inside the osseous cochlear tube. The helicotrema (conduit between scala tympani and scala vestibuli) is in subapical position, and the cochlear and lagenar ganglia and their associated nerve fibers are not enclosed by bone. In comparison, in extant therian mammals (i.e., marsupials and placentals) the helicotrema is located at the apex of the osseous cochlear canal, the three scalae coil to the same degree and the cochlear ganglion is enclosed by the primary bony lamina. Whether the lagenar ganglion is lost in therian mammals or integrated into the cochlear ganglion is still debated. The presence of a sensory lagenar macula at the apex of the membranous cochlear duct, innervated by a separate lagenar nerve and ganglion is a plesiomorphic condition of amniotes that monotremes share. A separate osseous lagenar canaliculus for the lagenar nerve, and the coiling of the distended lagenar sac at the end of the cochlear duct are autapomorphies of monotremes. Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra-otic cochlear ganglion suspended by membranous connective tissue. Among the major Mesozoic clades of crown mammals, cladotherians and gondwanatherians most likely acquired a fully functioning organ of Corti but lost the sensory lagenar macula, like extant therians. However, Mesozoic spalacotherioids, multituberculates and eutriconodonts likely retained the mammaliaform condition. J. Morphol. 278:236-263, 2017. © 2016 Wiley Periodicals,Inc.