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.

Gene, cell, and organ multiplication drives inner ear evolution

“…A second area of contention is the structural dissimilarity of the organ of Corti of all therians (Jahan et al, 2015a) and its evolution already in monotremes in terms of inner and outer hair cells (Chen and Anderson, 1985; Ladhams and Pickles, 1996) and their prestin motor (Okoruwa et al, 2008) separated by pillar cells with unusual molecular and structural features not found in other supporting cell type of any vertebrate (Jahan et al, 2015a). Importantly, in monotremes, the basilar papilla/organ of Corti resides in the lagena recess that has a lagena sensory epithelium at its tip that is entirely separated from the sound conducting perilymphatic space connected to the round and oval window (Schultz et al, 2016). Obviously, eutherian mammals lack a lagena, have a coiled cochlea with the organ of Corti extending to the apex, and have a continuous perilymphatic space (scala tympani, scala vestibuli) that provides the means for sound pressure propagation from the oval to the round window.…”

“…It evolved out of a less organized organ found in monotremes through reorganization of already specified inner and outer hair cells as a consequence of coiling related elongation that rearranged multiple rows of inner and outer hair cells of monotremes (Fritzsch et al, 2013; Schultz et al, 2016) into the single row of inner and three rows of outer hair cells of eutherian mammals (Lewis et al, 1985). Eliminating a single gene in mouse development, Foxg1, can alter the organ of Corti development to mimic that of monotremes in terms of shortening and rearrangement of hair cells into multiple rows (Fritzsch et al, 2013; Pauley et al, 2006) and similar effects can be achieved by altering convergent extension in PCP mutants (Jones et al, 2008).…”

The vertebrate middle and inner ear: A short overview

“…As then, dozens of studies focus on aspects of phylogeny (e.g., Benoit et al, 2015;Lebrun, De León, Tafforeau, & Zollikofer, 2010;Maisey, 2001), physiology (e.g., Armstrong, Bloch, Houde, & Silcox, 2011;Coleman & Colbert, 2007;Kirk & Gosselin-Ildari, 2009;Manoussaki et al, 2008), ontogeny (Billet, de Muizon, et al, 2015;Costeur, Mennecart, Müller, & Schulz, 2017;Ekdale, 2010;Mennecart & Costeur, 2016;Sánchez-Villagra & Schmelzle, 2007), paleobiology (e.g., David et al, 2010;Neenan & Scheyer, 2012;Pfaff Nagel, et al, 2017;Spoor, Bajpai, Hussain, Kumar, & Thewissen, 2002) or functional morphology (e.g, Coutier, Hautier, Cornette, Amson, & Billet, 2017;Grohé, Tseng, Lebrun, Boistel, & Flynn, 2016;Pfaff, Czerny, Nagel, & Kriwet, 2017b;Pfaff, Martin, & Ruf, 2015;Ruf et al, 2016;Schellhorn, 2018a;Schutz, Jamniczky, Hallgrímsson, & Garland, 2014;Spoor et al, 2007) of the labyrinth organ in extant but also extinct taxa. Anatomical correlations between membranous and bony labyrinths seem underrepresented, and precise and detailed descriptions based on histological serial and thin sections are valuable (e.g., Maier, 2013;Maier & van den Heever, 2002;Schultz, Zeller, & Luo, 2017;Starck, 1995;Wever, 1978Wever, , 1985.…”

“…Monotremes and early mammaliaforms show less than 360° (Luo, Ruf, & Martin, ; Luo, Ruf, Schultz, & Martin, ; Rowe, ; Ruf, Luo, & Martin, ; Ruf, Luo, Wible, & Martin, ). In monotremes, the cochlear apex containing the lagena is coiled and enlarged (Schultz et al, ), while gondwanatherian mammals show a short tapering cochlear canal with a slightly curved apex (Hoffmann, O'Connor, Kirk, Wible, & Krause, ). Therian mammals (marsupials and placentals) show at least one full turn but can have more than three turns (e.g., 3.25 in domestic cats [Schellhorn, ], or 3.3 in whales [Ekdale, ]).…”

Enhanced contrast in X‐ray microtomographic images of the membranous labyrinth using different X‐ray sources and scanning modes

“…; Schultz et al. ). Only a couple of authors have successfully visualised the membranous labyrinth yet (Uzun et al.…”