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Evolution of inner ear neuroanatomy of bats and implications for echolocation

Nature volume 602, pages 449–454 (2022)Cite this article

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Abstract

Phylogenomics of bats suggests that their echolocation either evolved separately in the bat suborders Yinpterochiroptera and Yangochiroptera, or had a single origin in bat ancestors and was later lost in some yinpterochiropterans1,2,3,4,5,6. Hearing for echolocation behaviour depends on the inner ear, of which the spiral ganglion is an essential structure. Here we report the observation of highly derived structures of the spiral ganglion in yangochiropteran bats: a trans-otic ganglion with a wall-less Rosenthal’s canal. This neuroanatomical arrangement permits a larger ganglion with more neurons, higher innervation density of neurons and denser clustering of cochlear nerve fascicles7,8,9,10,11,12,13. This differs from the plesiomorphic neuroanatomy of Yinpterochiroptera and non-chiropteran mammals. The osteological correlates of these derived ganglion features can now be traced into bat phylogeny, providing direct evidence of how Yangochiroptera differentiated from Yinpterochiroptera in spiral ganglion neuroanatomy. These features are highly variable across major clades and between species of Yangochiroptera, and in morphospace, exhibit much greater disparity in Yangochiroptera than Yinpterochiroptera. These highly variable ganglion features may be a neuroanatomical evolutionary driver for their diverse echolocating strategies4,14,15,16,17 and are associated with the explosive diversification of yangochiropterans, which include most bat families, genera and species.

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Fig. 1: Major neuroanatomical configurations of the spiral ganglion and Rosenthal’s canal in cochleas of bats.
Fig. 2: Evolutionary patterns and morphological disparity of Rosenthal’s canal and spiral ganglion in inner ears of bats.
Fig. 3: Apomorphic neuroanatomical configuration of wall-less Rosenthal’s canal (RC) for trans-otic ganglion in most Yangochiroptera, corroborating CT scans and histology in M. inflatus (Miniopteridae).

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Data availability

Skull specimens of bats and mammalian outgroups examined by CT scanning in this study are in the collection of Field Museum of Natural History, the teaching collections of UChicago, and the mammalogy collection of American Museum of Natural History. The specimen list is presented in Supplementary Table 2. CT scanning resolutions for all scanned specimens are listed in Supplementary Table 2. Metric measurements of CT visualization of the Rosenthal’s Canal and cochlear canal turns of these specimens are presented in Supplementary Table 3. Photographs of histological sections are presented in the figures and extended data figures.

Code availability

The metric measurements of the Rosenthal’s canal and cochlear turns were obtained using the Mimics visualization package (www.materialise.com). Methods of morphological disparity analysis and ancestral state reconstruction are presented in the Supplementary Information.

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Acknowledgements

This research was supported by UChicago Metcalf Fellowship and Graduate Fellowships from NSF and AMNH (to R.B.S.), by Postdoctoral Fellowships from NSF and University of Illinois (to D.J.U.), Field Museum Brown Mammal Research Fund and grant from JRS Biodiversity Foundation (to B.D.P.) and UChicago Biological Sciences Division and NSF fundings (to Z.-X.L.). We thank J. Schultz, K. Sears, N. Simmons, G. Manley, R. MacPhee and J. Flynn for discussion; K. Sears and E. Rodriguez for access to histological sectioning facilities. Full acknowledgements are presented in the Supplementary Information.

Author information

Authors and Affiliations

  1. Richard Gilder Graduate School, American Museum of Natural History, New York, NY, USA

    R. Benjamin Sulser

  2. Negaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA

    Bruce D. Patterson

  3. Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Daniel J. Urban

  4. The Sears Lab, Department of Ecology and Evolution, University of California Los Angeles, Los Angeles, CA, USA

    Daniel J. Urban

  5. Department of Organismal Biology and Anatomy, The University Chicago, Chicago, IL, USA

    April I. Neander & Zhe-Xi Luo

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Contributions

Conceptualization: R.B.S., Z.-X.L. and B.D.P. Data contribution: all authors. CT scanning: A.I.N. and R.B.S. CT visualization and morphometrical analysis: R.B.S. Histological sections: R.B.S. and D.J.U. Providing access to museum collections and histological specimens: B.D.P. Interpretation of anatomical data: R.B.S., Z.-X.L., B.D.P. and A.I.N. Compilation of Supplementary Information: R.B.S., Z.-X.L. and B.D.P. Graphics: R.B.S., A.I.N. and Z.-X.L. Writing: R.B.S., Z.-X.L. and BDP, and approved by all authors. The project was coordinated by Z.-X.L.

Corresponding authors

Correspondence to R. Benjamin Sulser or Zhe-Xi Luo.

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Nature thanks Brock Fenton, Amanda Lauer and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Phylogenetic evolution and systematic character distribution of the wall patterns of Rosenthal’s canal for placement of the spiral ganglion among bats and outgroups, showing phylogeny and classification.

A (left, cladogram): phylogeny of Chiroptera (tree topology based on Ref. 35.-Shi and Rabosky, 2015) Superfamilies are indicated by numbers: 1- Rhinolophoidea, 2- Emballonuroidea, 3 - Noctilionoidea, 4 - Vespertilionoidea. B.-D. (right columns), wall patterns of Rosenthal’s canal (RC) from the basal ½ turn to the third (apical) turn of the entire cochlea (explanation: between the fenestra vestibuli and basal ½ turn landmark, the spiral ganglion canal has small foramina in all therian mammals, and no variation in the local area). The research here focuses on the structural and phylogenetic variations in ganglion canal wall between the basal ½ turn and the apex). B. RC wall pattern at the basal ½ cochlear turn; C. RC wall pattern at the 1.5 cochlear turn; D. RC wall pattern at the 2.5 cochlear turn. For taxa with less than 2.5 turns, the patterns in the remainder of coil from turn 1.5 onward is represented. The three major wall patterns (lower left panel) are explained in Fig. 1 and Extended Data Fig. 2. Structures of the cochlear canal and the spiral ganglion canal are based on CT scanning (Supplementary Tables 1–3; n = 45). Of these, 15 bats and two outgroups are examined both by CT scans and then corroborated by original histological sections of this study, or from published histological literature (Supplementary Table 1). Symbol † - two taxa (Homo sapiens and Crocidura russala) that are based on published cochlear structure from literature. E. Echolocation duty cycle for bats in this study (LDC= Low Duty Cycle, HDC = High Duty Cycle). Foraging habitats and foraging modes of bats. Abbreviations for foraging habitats for echolocation: E –around the edges of open space; Nc – narrow space with cluttered background; O - open and uncluttered foraging space (Ref. 42.- Denzinger and Schnitzler 2013); TC - tongue-clicking echolocation. Abbreviations for foraging modes: A – aerial foraging of insects; Fr – frugivorous; Fl –foraging for fluttering insects; G- gleaning for prey; Tw – trawling over water.

Extended Data Fig. 2 Ancestral state reconstruction for the wall configurations of Rosenthal’s canal of bats and therian mammal outgroups. Each taxon is assigned a diagnostic character in one of the three major canal wall patterns.

The assignments were based on one of the two alternative representation schemes. A. The wall structure of the ganglion canal of each taxon is represented by the most derived ganglion wall pattern for taxa with multiple patterns. B. The most extensive canal wall pattern (character state), ranked by the highest percentage to the total cochlear length, is assigned to be the diagnostic character of the taxon. The ancestral state reconstruction at the main nodes of the cladogram is estimated by utilizing the phytools (Ref. 45 - Revell 2012) and ape (Ref. 46 - Paradis and Schliep, 2019) programs in R (Ref. 47 - R core team, 2013). The foraminal wall with cis-otic ganglion (Blue - primitive); the fenestral wall and cis-otic ganglion (Green - intermediate); the wall-less canal and trans-otic ganglion (Red – most derived). Tree topology is adapted from Shi and Rabosky (2015) (Ref. 35.) and Teeling et al. (2016). C. Morphological disparity of the inner ear ganglion by the enclosure of the cochlear ganglion (measured via percent ossification, see main text) and cochlear turns. Symbols and plot are identical to Fig. 2, but adjusted to show alternate groupings of Yangochiroptera (red) and Yinpterochiroptera + outgroups (blue). Source data in Supplementary Table 3.

Extended Data Fig. 3 Three major neuroanatomical configurations of the spiral ganglion and Rosenthal’s canal in bats and therian outgroups.

A. Schematic configuration of Rosenthal’s canal, its tractus foraminosus (= foraminal wall), and their structural relationships to the cochlear nerve fiber fascicles and the cis-otic ganglion placement. B. Schematic model of the bony canal for the cis-otic ganglion and the foramina on the surface of internal auditory meatus (nerve structures omitted for clarity). B1. Felis catus (mammal outgroup; domestic cat): the foraminal canal wall structure as seen on the surface of the internal auditory meatus, visualized by CT. B2. Hypsignathus monstrosus (Yinpterochiroptera, Pteropodidae) – the hammer-headed bat: the foraminal RC wall in the internal auditory meatus. B3. Rhinolophus blasii (Yinpterochiroptera, Rhinolophidae) Blasius’s horseshoe bat: the foraminal RC wall in the internal auditory meatus. The foraminal configuration (B1 - B3) is typical of therian mammals and plesiomorphic for Chiroptera as a group and for Yinpterochiroptera. C and C1. Tadarida brasiliensis (Yangochiroptera, Molossidae) – the Brazilian free-tailed bat: the fenestral configuration with large openings (tractus fenestralis) in the thinner wall with the cis-otic placement of the spiral ganglion. The large fenestra typically are present in the basal and near the ½ cochlear turns in bats having this pattern. The fenestral pattern is more derived than the plesiomorphic foraminal pattern, and it is an intermediate character state between the foraminal pattern and the most derived wall-less pattern. D and D1. Miniopterus inflatus (Yangochiroptera, Miniopteridae) – the greater long-fingered bat: the wall-less pattern of Rosenthal’s canal, typically between the apex and the basal ½ cochlear turn, allows the trans-otic placement of the spiral ganglion, making ganglion space confluent with the space of the internal auditory meatus in the absence of RC wall. With the exception of the species of Noctilio, all Yangochiroptera show this pattern in the apical turn of the cochlea (Extended Data Fig. 1). Structurally, this is the most extreme neuroanatomical pattern of the ganglion and its canal. The confluence of spiral ganglion space and the internal auditory meatus eliminates the constraint of many small foramina for the cochlear nerve fascicles to connect to the spiral ganglion and helps to shorten the ganglion’s connection to cochlear nerve trunk. It also provides more space to accommodate greater numbers of ganglion neurons in higher density.

Extended Data Fig. 4 Therian outgroup (Felis catus) and yinpterochiropteran bats (Epomophorus wahlbergi and Rousettus aegyptiacus): foraminal wall of the Rosenthal’s canal (RC) for cis-otic ganglion placement.

A. Schematic illustration of the cochlear nerve fiber fascicles and the cis-otic spiral ganglion, and their anatomical relationships to osteological structures. A1. The tractus foraminosus (foraminal wall) extends from the base to the apex of the cochlea, shown as dense foramina in the wall of internal auditory meatus in a schematic uncoiled cochlea. Yinpterochiropteran bats (Epomophorus – non-echolocating and Rousettus – tongue-clicking echolocation) have the plesiomorphic foraminal wall and cis-otic ganglion placement, as in non-chiropteran therian mammals (represented by Felis catus, Carnivora, Laurasiatheria). B. Epomophorus wahlbergi: Histological section through modiolar section of the whole cochlea. B1. Histological details at basal ½ cochlear turn. C. Epomophorus - CT visualization of location of the ganglion in a transparent cochlea, with CT slice through to visualize the relationship of the ganglion. C1. Cut-away CT model the modiolar section of the cochlea to show the tractus foraminosus and ganglion (yellow) in Rosenthal’s canal, relative to the cut-away internal auditory meatus. D. Epomophorus CT slice through the modiolar section of the cochlea to illustrate the osteological structures of the ganglion and cochlear nerve fibers (corresponding to histological section of B). D1. Details of the cochlea and Rosenthal’s canal at the 1/2 cochlear turn. E. Rousettus aegyptiacus – CT slice across the modiolar plane of the cochlea to show the foraminal wall pattern of Rosenthal’s Canal in the entire internal auditory meatus. E1. Details of ossified foraminal wall of the Rosenthal’s canal at basal ½ turn of Rousettus. F. Felis catus (representative of laurasiatherian outgroup) - Cut-away CT visualization model of foramina on the ossified wall of the internal auditory meatus, and the inclusion of the ganglion (yellow) in Rosenthal’s canal. F1. Felis – CT slice through modiolar plane to show details of Rosenthal’s canal and its foraminal wall, relative to the internal auditory meatus. G. CT slice through the entire cochlea at the modiolar section. G1. Felis – enlarged details of Rosenthal’s canal and its structures at the basal 1.2 cochlear turn. The tractus foraminosus in the internal auditory meatus, the foraminal wall of the ganglion canal, and the internal placement of cis-otic ganglion are the ancestral pattern of therians, and their Mesozoic dryolestoid relatives (Ref. 22.- Luo et al. 2012). These are plesiomorphic for laurasiatherian placentals, including Felis catus and all yinpterochiropteran bats.

Extended Data Fig. 5 Histology and CT scans of neuroanatomy of Rosenthal’s canal for the cis-otic spiral ganglion in Hipposideros caffer (Yinpterochiroptera, Hipposideridae).

Sundevall’s roundleaf bat is a laryngeal echolocating bat. A. Diagram of the foraminal wall of Rosenthal’s canal for cis-otic placement of the ganglion, showing the tractus foraminosus (foraminal wall pattern) for the fascicles of cochlear nerve to connect with the ganglion in the Rosenthal’s canal; A1. Distribution of foramina along the length of cochlea. B. Histological section at the modiolus, to show internal auditory meatus, the canaliculi of tractus foraminosus in the entire cochlea; B1, Histological structures of the spiral ganglion in Rosenthal’s canal, the cochlear nerve fascicles through canaliculi of tractus foraminosus, and the radial fibers of the ganglion through the habenula perforata in the primary bony lamina, at the 1½ cochlear turn. C. and C1. CT scan slice through the modiolar section, corresponding to histology section of B and B1: to show the ganglion space in Rosenthal’s canal, the tractus foraminosus in canal wall, and the habenula perforata in primary bony lamina for radial ganglion fibers at the 1½ cochlear turn. D and D1. CT slice through transparent model, and cut-away section corresponding to histological section, to show the foraminal pattern on the surface of the internal auditory meatus near the 1½ to 2 cochlear turns. E. Cut-away CT visualization of the whole cochlea at the modiolar section. E1. Intact cochlea in the medial (endocranial) view of the internal auditory meatus to show the foraminal wall pattern.

Extended Data Fig. 6 Foraminal Rosenthal’s canal and cis-otic placement for two yinpterochiropteran LDC echolocators, Rhinopoma hardwickii and Lyroderma lyra.

A. Anatomy of key neural and osteological structures. A1. Distribution of foramina for cochlear nerve fascicles from the base to the apex of the cochlea. B. Rhinopoma – uCT sections through the modiolar section of the whole cochlea. B1. Detail of Rosenthal’s canal at the first ½ turn of the cochlea. C. Transparent inner ear model with the spiral ganglion (yellow) visible. C1. and C2. Cut-away section of the inner ear model to visualize the location of the spiral ganglion in relation to Rosenthal’s canal. D. Details of the inner ear model in the medial (endocranial) view to visualize the extent of ossification within the modiolar region. E. Lyroderma lyra (“Megaderma lyra”)- transparent inner ear model with the spiral ganglion (yellow) visible. E1. and E2. Cut-away section of the inner ear model to visualize the location of the spiral ganglion in relation to Rosenthal’s canal. F uCT sections through the modialor section of the whole cochlea. F1. Detail of Rosenthal’s canal at the first ½ turn of the cochlea. G. Details of the inner ear model in the medial (endocranial) view in order to visualize the extent of ossification within the modiolar region.

Extended Data Fig. 7 Histology and CT scans of neuroanatomy of Rosenthal’s canal for fenestral wall of Rosenthal’s canal for the Cis-otic Spiral Ganglion in Coleura afra (Yangochiroptera, Emballonuridae).

The African sheath-tailed bat Coleura afra is a laryngeal echolocating bat of Yangochiroptera. A. Diagram of the fenestral wall (tractus fenestralis) of Rosenthal’s canal (RC); the large fenestrae of RC wall are well developed beyond the basal ¾ turn, and the RC becomes wall-less in the apical ½ turn. The basal-most part of the cochlea retains the standard mammalian pattern of small foramina. B. Histology section through the modiolar plane and the internal auditory meatus to show the cis-otic placement of the ganglion, the tractus fenestralis that forms the canal wall. B1. Histological details of the fenestral openings of the 1½ cochlear turn. C. CT scan slice corresponding to the histological section of the whole cochlea. C1. CT visualization of the ganglion space in Rosenthal’s canal and the fenestral openings in canal wall at the 1½ cochlear turn. D. Transparent cochlea and D1. Cut-away section corresponding to histological sections (B and B1): the fenestras in the internal auditory meatus near the 1 to 1½ cochlear turns, and wall-less pattern of the apical turn. E. Intact cochlea in the medial (endocranial) view of the internal auditory meatus to show the fenestral wall pattern. E1. Cut-away CT visualization of the whole cochlea at the modiolar section.

Extended Data Fig. 8 Fenestral wall of Rosenthal’s canal and cis-otic placement of ganglion in Tadarida brasiliensis (Yangochiroptera, Molossidae) by CT scans.

The Brazilian free-tailed bat Tadarida brasiliensis is a laryngeal echolocating bat. A. Diagram of the fenestral wall of Rosenthal’s canal. A1. The canal wall shows large fenestrae between the basal ½ turn and 1½ turn, but it becomes wall-less in the apical ½ turn. B. and C. Outline illustration and CT scan slice across the modiolar section of the fenestral pattern up to ½ turn and the wall-less pattern in apical ½ turn. C1. Details of the large fenestral opening (tractus fenestralis) between the RC canal and the internal auditory meatus. D and D1. Transparent CT visualization and cut-away section of local details of fenestrae in the internal auditory meatus. E. Intact cochlea in the medial (endocranial) view of the internal auditory meatus to show the fenestral wall; and E1. Modiolar section to show the continuous variation of fenestral pattern (up to 1½ turn) and the wall less pattern (the apical ½ turn) along the length of the cochlea.

Extended Data Fig. 9 Yangochiropteran vesper bats Pipistrellus abramus (Vespertilionidae) and Myotis lucifugus (Vespertilionidae): wall-less Rosenthal’s canal with trans-otic placement of spiral ganglion.

The Japanese pipistrelle bat (P. abramus) and the Little brown bat (M. lucifugus) are laryngeal echolocating bats. Their neuroanatomical RC and ganglionic patterns are the most derived characters among mammals, only known in yangochiropterans. A. Schematic diagram to show the absence of Rosenthal’s canal wall and the confluence of the ganglion with cochlear nerve in internal auditory meatus (IAM). A1. Rosenthal’s canal has no wall between the basal ½ turn and apex, although the basal most ½ turn has foramina. B and B1. Histological section of Pipistrellus showing the spiral ganglion is placed in IAM, starting from near the base of the cochlea (Ref. 48 - Hsiao et al. 2015: fig. 2. Histological section reproduced with permission/license from Copyright Clearance Center: www.rightfind.com). C. and C1. CT slice through the modiolar section to show that Rosenthal’s canal wall is entirely absent from the basal ½ to the apex; and the presumptive position of the ganglion is in IAM. D. Transparent model of cochlea to visualize the position of the ganglion. D1. Solid CT model of cochlea cut away at the modiolar section visualize the wall-less condition of Rosenthal’s canal space and the placement of spiral ganglion in IAM. E. Myotis - Transparent cochlea to visualize the spiral ganglion space (yellow). E1. Cut-away surface to visualize that the ganglion space is open and confluent with the IAM. E2. Cut-away model to show the open and confluent condition of Rosenthal‘s canal of the entire internal auditory meatus. E3. Solid cochlea model of the internal auditory meatus to show the exposure of the spiral ganglion. F. Myotis - CT slice through the modiolar section. F1. Detailed osteological structures at 1½ turn. F2. Detailed osteological structure at the cochlear base. F3. Detailed osteological structures at 1½ turn. C. Transparent model of the cochlea. Abbreviations: bm – basilar membrane; IAM – internal auditory meatus; RC – Rosenthal’s canal; sg – spiral ganglion; sm – scala media; st – scala tympani; sv – scala vestibuli; tcm – tectorial membrane; TF – tractus foraminosus; vm – vestibular membrane.

Extended Data Fig. 10 Wall-less Rosenthal‘s canal for trans-otic placement of the spiral ganglion of Pteronotus parnellii (Yangochiroptera, Mormoopidae) - Parnell’s mustached bat, a laryngeal echolocating bat.

A. Schematic model of osteological structures. A1. Uncoiled schematic cochlea to visualize the wall-less part of Rosenthal’s Canal between the basal ½ turn and the apical turn. B. Whole mount prepared nerve structures in the basal cochlear turn: cochlear nerve trunk, cochlear nerve fiber fascicles, spiral ganglion, and ganglion radial fibers to hair cells (image redrawn from Henson and Henson 1988: fig. 1) (Ref. 10). C. CT slice corresponds to whole-mount cochlear nerve dissected (B) and visualizes the foraminal wall of Rosenthal‘s canal in the basal ½ turn, and the absence of the wall of Rosenthal‘s canal beyond basal ½ turn. The absence of Rosenthal’s canal wall at ½ turn is corroborated by histology (Ref. 30 - Kössl and Vater 1985: fig. 1). D. Transparent inner ear model with location of the spiral ganglion (yellow). D1. Modiolar section of cochlea: Spiral ganglion is positioned in the internal auditory meatus between the basal ½ turn and the apex. D2. Details in modiolar section to visualize that the space of the ganglion is open and confluent with the IAM. E. CT visualization of the internal auditory meatus.

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Sulser, R.B., Patterson, B.D., Urban, D.J. et al. Evolution of inner ear neuroanatomy of bats and implications for echolocation. Nature 602, 449–454 (2022). https://doi.org/10.1038/s41586-021-04335-z

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