Downloaded from rspb.royalsocietypublishing.org on November 27, 2010 Fossil evidence on evolution of inner ear cochlea in Jurassic mammals Zhe-Xi Luo, Irina Ruf, Julia A. Schultz and Thomas Martin Proc. R. Soc. B 2011 278, 28-34 first published online 28 July 2010 doi: 10.1098/rspb.2010.1148 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2010/07/26/rspb.2010.1148.DC1.h tml References This article cites 34 articles, 6 of which can be accessed free http://rspb.royalsocietypublishing.org/content/278/1702/28.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections palaeontology (134 articles) developmental biology (212 articles) evolution (2221 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions This journal is © 2011 The Royal Society Downloaded from rspb.royalsocietypublishing.org on November 27, 2010 Proc. R. Soc. B (2011) 278, 28–34 doi:10.1098/rspb.2010.1148 Published online 28 July 2010 Fossil evidence on evolution of inner ear cochlea in Jurassic mammals Zhe-Xi Luo1,2,*, Irina Ruf2, Julia A. Schultz2 and Thomas Martin2 1Section of Vertebrate Paleontology, Carnegie Museum of Natural History, Pittsburgh, PA 15213, USA 2Steinmann-Institut fu¨r Geologie, Mineralogie und Pala¨ontologie, Universita¨t Bonn, 53115 Bonn, Germany The coiled cochlea is a key evolutionary innovation of modern therian mammals. We report that the Late Jurassic mammal Dryolestes, a relative to modern therians, has derived bony characteristics of therian-like innervation, but its uncoiled cochlear canal is less derived than the coiled cochlea of modern therians. This suggests a therian-like innervation evolved before the fully coiled cochlea in phylogeny. The embry- ogenesis of the cochlear nerve and ganglion in the inner ear of mice is now known to be patterned by neurogenic genes, which we hypothesize to have influenced the formation of the auditory nerve and its ganglion in Jurassic therian evolution, as shown by their osteological correlates in Dryolestes, and by the similar base-to-apex progression in morphogenesis of the ganglion in mice, and in transformation of its canal in phylogeny. The cochlear innervation in Dryolestes is the precursory condition in the curve-to- coil transformation of the cochlea in mammalian phylogeny. This provides the timing of the evolution, and where along the phylogeny the morphogenetic genes were co-opted into patterning the cochlear innervation, and the full coiling of the cochlea in modern therians. Keywords: Mammalia; inner ear; evolution; Jurassic 1. INTRODUCTION stem taxon characterized by plesiomorphic dental fea- The snail-shaped cochlea with its hearing organ (Organ of tures, and a near relative to the modern marsupials and Corti) is a key evolutionary innovation in the inner ear of placentals. The fine inner ear structures are preserved in modern marsupial and placental mammals. Coiling of the a petrosal bone that houses the inner ear in the skull. cochlea is a major feature distinguishing the modern mar- Through the high-resolution micro-computer tomo- supials and placentals from all other mammals [1–5]. graphy (CT) scanning and comparative analysis, we The cochlea coils into a spiral to compact itself into a obtained new information on its morphological features smaller space in the skull for efficient innervation and that represent the evolutionarily ancestral condition of blood supply in marsupials and placentals [6,7]. extant therian mammals. This is relevant to the under- Elongation of the cochlea with more spiral turns is corre- standing of the evolution of the coiled cochlear canal and lated with increased resolution of sound frequencies the innervation of its hearing organ. [2,8]. The curved gradient of the coiled cochlear canal wall focuses acoustic energy towards the apex of the cochlea, the most sensitive region for the low-frequency 2. MATERIAL AND METHODS sound [9]. The key innovation in the fully coiled cochlea, The petrosal specimen (Guimarota Collection of Museo including its auditory innervation, is correlated with the Geolo´gico (Lisboa, Portugal), specimen number SGP earliest diversification of metatherians and eutherians in 6807) shows similar apomorphic features as the known pet- the Cretaceous, and has led to many spectacular func- rosal of the paurodontid Henkelotherium (Paurodontidae, tional adaptations in hearing in Cenozoic and living Dryolestoidea) [5,18]. The inner ear inside the petrosal marsupials and placentals [3,5,10–16]. However, evol- was observed by our high-resolution micro-CT scanning ution of this important ear structure cannot be fully and visualized by three-dimensional virtual endocasts from deciphered until the precursory condition of its main the CT data. characters can be mapped from the fossil record of The first scanning of X-ray CT was by the OMNI-X early therians, and their phylogenetic transformation Universal HD600 Scanner at the Center of Quantitative can be correlated with the morphogenesis patterned by Imaging (CQI), Pennsylvania State University, State Col- developmental genes. lege, Pennsylvania, USA. The images have a 1024 pixel Here, we report the discovery of the precursory struc- resolution and voxel size of 0.025 Â 0.025 Â 0.028891 mm. tures of the fully coiled cochlea of modern therians in the This scanning allowed us to initially identify this fossil. inner ear of the Late Jurassic mammal Dryolestes leiriensis The second scanning for greater morphological details was [17], a 150 Myr old fossil mammal in the cladotherian by scanner vjtomejx s (GE Sensing & Inspection Technol- clade, as defined by the common ancestor of ogies GmbH phoenixjx-ray) at the Steinmann-Institut fu¨r dryolestoids þ extant therians (e.g. [3]). Dryolestes is a Geologie, Mineralogie und Pala¨ontologie, Universita¨t Bonn, Germany. The images have a 1024 pixel resolution and a voxel size of 0.010158 Â 0.010158 Â 0.010158 mm. * Author for correspondence ([email protected]). To increase the resolution of the region of interest (cochlear Electronic supplementary material is available at http://dx.doi.org/10. canal), we used the software datosjx-reconstruction (GE 1098/rspb.2010.1148 or via http://rspb.royalsocietypublishing.org. Sensing & Inspection Technologies GmbH phoenixjx-ray) Received 28 May 2010 Accepted 6 July 2010 28 This journal is q 2010 The Royal Society Downloaded from rspb.royalsocietypublishing.org on November 27, 2010 Inner ear evolution of mammals Z.-X. Luo et al. 29 Table 1. Measurement of bony labyrinth structures of D. leiriensis (SGP 6807). (Endocast measurements from AVIZO 5.1 based on the second CT scanning in the scanner in Steinmann-Institut, Universita¨t Bonn. Scanned resolution 0.010158 mm; virtually half voxel size 0.005079 mm.) coiling along length estimated length (mm) cochlear canal 2708 3.3 primary bony lamina length 1.6 secondary bony lamina length 1.18 long diameter (mm) short diameter (mm) fenestra vestibuli 0.53 0.47 estimated diameter width (mm) height (mm) (width–height average mm) apical turn diameter 0.77 0.85 0.68 basal turn diameter 0.99 0.96 1.2 angle of basal turn to lateral 1458 semicircular canal semicircular canals width (mm) height (mm) arc radius lumen (inner curvature mm) diameter (mm) anterior 2.31 2.22 1.13 0.21 posterior 1.56 1.50 0.77 0.22 lateral 1.55 1.46 0.75 0.22 average radius 0.88 for virtually halving the voxel size (0.005079 mm) from the have gliding, flying, saltatorial or fully aquatic loco- raw dataset, which has further increased the resolution of motion. Dryolestes was either a generalized terrestrial, or fine structures (electronic supplementary material, figures a scansorial mammal, neither of which can be ruled out S2–S3). Virtual reconstructions of the petrosal bone and because its postcranial skeleton is not preserved, except the inner ear bony labyrinth were completed by manual for a single humerus [22]. But the latter possibility of a segmentation function of the software AVIZO 5.1. Linear scansorial mammal is more likely by comparison to the measurements were from the inner ear bony labyrinth closely related dryolestoid Henkelotherium, which has endocast with Avizo (table 1). many scansorial skeletal features [18]. (b) Cochlear canal structure 3. DESCRIPTION AND COMPARISON The cochlear canal in Dryolestes is 3.3 mm long and partly (a) Vestibule and semicircular canals coiled through about 2708 or three-quarters of a complete On the three-dimensional virtual endocasts visualized turn, starting from the proximal entry point of the from the CT scanning, the vestibular part of the inner cochlear nerve (figures 1, 2 and table 1), according the ear shows a discernible separation between the utricle measurement landmarks suggested by West [8] (see also and the saccule of the vestibule (figure 1d–f ), the fenestra [5,23]). The canal is relatively straight and has a circular vestibuli (with a stapedial ratio of 1.2), which transmits cross section near the base. Its distal half-turn forms an sound into the inner ear, and the fenestra cochleae for arc around the distal point of the cochlear nerves and releasing the sound pressure (figure 1). The anterior, pos- has an oval cross section in the apical part. The curvature terior and lateral semicircular canals for the detection of of the cochlear canal corroborates previous observations motion and equilibrium function have their respective that the pre-tribosphenic mammals, such as Henkelother- arc radii at 1.13, 0.75 and 0.77 mm (figure 1: asc, lsc ium [ 5] and Vincelestes [24], have a consistent, and psc). The plane of the lateral semicircular plesiomorphic pattern of 2708 curvature of cochlea canal forms a 1458 angle to the axis through the basal (three-quarters of a turn).