Functional morphological adaptations of the bony labyrinth in marsupials (Mammalia, Theria)

Abstract

Diprotodontia represents the largest and ecologically most distinct order of marsupials occurring in Australasian being highly divers in size, locomotion, habitat preferences, feeding, and activity pattern. The spatial orientation in the habitat and therefore the three-dimensional space is detected by the vestibular system of the inner ear, more precisely by the three semicircular canals. In this study, we investigated the bony labyrinth of diprotodontian and selected non-diprotodontian marsupial mammals of almost all genera with noninvasive micro-CT scanning and 3D-reconstructions. In principal component analyses, the subterranean taxon can be separated from gliding and saltatorial taxa, whereas arboreal species can be separated from saltatorial specimens. The highest PCA loadings of this functional distinction are clearly found in the diameter of the semicircular canals, whereas the overall shape (height, width, length) of the semicircular canals is less important. Additionally, the investigated arboreal and fossorial species of South America are nested in the morphospace of the Australasian taxa. Even if a phylogenetic signal in the anatomy of the bony labyrinth cannot be excluded entirely, the main functional morphological signal of the vestibular system is found in the diameter of the semicircular canals. With the large dataset of extant marsupial mammals analysed here, the locomotion mode of extinct taxa can be inferred in future studies independent of any evidence of postcranial material.

Neuroanatomy of the spinosaurid Irritator challengeri (Dinosauria: Theropoda) indicates potential adaptations for piscivory

“…Endolymphatic flow within the inner ear organ is determined by semicircular canal geometry, and the shape of the vestibular organ is therefore expected to vary depending on locomotor mode, as has been found for many mammal groups [e.g. [51][52][53][54] ]. www.nature.com/scientificreports www.nature.com/scientificreports/ Functional changes in vestibular anatomy are expected to be largest in groups that experienced strong ecological transitions, such as the evolution of secondarily marine lifestyles or flight.…”

Visualization of the Membranous Labyrinth and Nerve Fiber Pathways in Human and Animal Inner Ears Using MicroCT Imaging

“…Non-destructive microCT imaging has been extensively used in the past years to visualize anatomical details of inner ear samples and to assess morphometric variations. So far, most of these studies focused on the bony structure and did not take into account soft tissue ( Van Spaendonck et al, 2000 ; Wimmer et al, 2014 ; Schurzig et al, 2016 ; Ni et al, 2017 ; Pfaff et al, 2017 ). Visualization of the delicate membranous labyrinth and main nerve fibers in the inner ear is of great importance for any study to assess geometric variability to design new electrodes for electrical stimulation.…”

The vertebrate middle and inner ear: A short overview

“…In the early 1980s, the investigation of fragile fossil material with destructive methods was increasingly replaced by noninvasive computer tomography scanning (e.g., Conroy & Vannier, 1984;Hoffmann, Schultz, et al, 2014a), which provides a method to virtually reconstruct the internal anatomy of the bony labyrinth. 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, 1978…”

“…Even though Hyrtl (1873) doubted any correlation between the structure of the vestibular system and locomotion type, recent functional investigations of the inner ear morphology in a variety of vertebrates based on micro-CT scanning clearly show that shape and locomotion are linked (e.g., Berlin, Kirk, & Rowe, 2013;Billet et al, 2012;Cox & Jeffrey, 2010;David et al, 2010;Malinzak, Kay, & Hullar, 2012;Pfaff et al, 2015;Pfaff, Czerny, et al, 2017b;Ryan et al, 2012;Spoor et al, 2007;Spoor, Wood, & Zonneveld, 1994;Spoor & Zonneveld, 1998). Even though, the results of these studies appear controversial between different orders (e.g., functional-morphological distinction based on size of SCs vs. diameter of SCs), the diameter and arc size of the SCs are positively correlated among vertebrates and are not independent from one another (Muller, 1999).…”