Anatomical variations in hearing and sound production in amniotes

Abstract

Vertebrates use their senses to interact with their environments through a diverse array of behaviours that are underpinned by an equally expansive suite of adaptive features, which redeploy evolutionarily ancient sensory cell types (Schlosser, 2018). In this special issue of the Journal of Anatomy, our authors present novel data on some of the remarkable sensory features of birds, mammals and reptiles. This collection of studies captures aerial, terrestrial and aquatic sensory capabilities, across both extant and extinct taxa. Collectively, the authors illuminate soft and hard tissue features of the auditory and vocal apparatus using a suite of imaging and analytic techniques, besides presenting novel behavioural and kinematic data to capture the dynamic and emergent properties of sensory input.

Beginning with bats, the second most diversified group of mammals (Simmons, 2005) and the only group to have coupled self-powered flight (Rayner, 1988) with echolocation, our issue includes two detailed examinations of craniofacial development (Meguro et al., 2024; Pommery et al., 2024). These authors focus on the upper jaw complex (Pommery et al., 2024) and the orofacial complex (Meguro et al., 2024) in relation to the remarkable ability of bats to engage in laryngeal echolocation, an example of ‘active sensing’ (Nelson & MacIver, 2006) that allows bats to probe both the vast night sky and the complicated geometry of cave environments. Most bats produce high-frequency vocalisations and use their auditory apparatus to perceive the reflected echoes from their environment. Captured auditory information is then processed in specific regions of the brain (Teeling, 2009) allowing bats to navigate and hunt in pitch darkness. Several aspects of this astounding sensory system have been investigated. Particularly, recent studies in the fields of anatomy and evolutionary morphology, facilitated by micro-Computed Tomography (microCT) and diffusible iodine contrast-enhanced staining of soft tissues (Gignac et al., 2016), have assessed the patterning and magnitude of variation in features of the inner ear (e.g. Davies et al., 2013; Nojiri et al., 2021, 2024; Sulser et al., 2022) and larynx (e.g. Brualla et al., 2024; Carter, 2020; Snipes & Carter, 2022). Here, Meguro and colleagues (Meguro et al., 2024) shift focus to present novel three-dimensional descriptions of embryonic orofacial development, examining the development of orofacial clefting, which has been suggested to have a functional role in echolocation (Arbour et al., 2019; Curtis et al., 2020; Orr et al., 2016). With an evolutionary sample, Meguro et al. (2024) characterize orofacial morphotypes among non-laryngeal echolocators, oral- and nasal-emitting laryngeal echolocators, comprising novel descriptions of bone, cartilage and epithelial organs. The authors demonstrate that cleft morphology arises through heterogeneous developmental pathways in oral- and nasal-emitting laryngeal echolocating bats (Meguro et al., 2024). Their study highlights the diversification of the orofacial complex in bats and draws parallels between bat orofacial morphotypes and submucosal cleft palate in humans, which warrants further investigation. Pommery and colleagues (Pommery et al., 2024) add further novel data on prenatal growth and development of the palatine bones in bats, along with the other constituent elements of the upper jaw complex, the premaxilla, maxilla and vomer. The authors focus on quantifying evolutionary patterns of allometry for these cranial elements across a broad sample of bats and non-bat mammals. The magnitude of variation in patterns of prenatal ontogenetic allometry in mammals is poorly known relative to postnatal patterns. Here, Pommery and colleagues (Pommery et al., 2024) identify significant differences in prenatal ontogenetic allometry among bats, a high magnitude of variation in ossification timing of the premaxilla, and several shifts in the timing of bone ossification for nasal- compared to oral-emitting echolocators. These results provide novel insight into the variation in the development of the upper jaw complex in bats that may be linked to their high level of craniofacial diversity.

Echolocation capabilities are present in other mammals besides bats. In the case of toothed whales (Odontoceti), the capacity to echolocate supports hunting, navigating and communicating in an aquatic environment (Geisler et al., 2014). The evolution of echolocation in odontocetes has resulted in extensive restructuring of auditory structures and reorganisation of neural pathways associated with hearing (Berns et al., 2015), along with the appearance of specialised craniofacial features, such as retrograde cranial telescoping (Churchill et al., 2018). Echolocation has been reconstructed as likely evolving in odontocetes during the Oligocene (~30Mya), with fossil archaic odontocetes bearing features of the inner ear consistent with extant members of the clade, and supporting high-frequency hearing (e.g. Churchill et al., 2016). In this issue, Racicot and colleagues (Racicot et al., 2024) examine the endosseous labyrinth of the inner ear and quantify cochlear morphology in a sample of extant and extinct odontocetes. Through tracing features of ear ossicle shape using 3D models derived from microCT data, Racicot et al. (2024) uncover an early evolution of the ability to hear narrow-band, high-frequency (NBHF) sounds. The authors hypothesise that this capacity was present in the early Oligocene and in stem members of Delphinidae (ocean dolphins) in the early Miocene. Among extant odontocetes, the capacity to hear NBHF sounds appears in multiple differently related groups, considered convergent evolution of a predatory avoidance strategy (Andersen & Amundin, 1976; Galatius et al., 2019; Morisaka & Connor, 2007). Novel data and analyses presented by Racicot et al. (2024) suggest this hearing capacity may be an ancestral feature of the clade.

Traveling further back in the fossil record of cetaceans, Corrie and Park (2024) turn our attention to the little-known auditory capabilities of stem cetaceans (Archaeocetes) belonging to the group Kekenodontidae, from the late Oligocene. The clade represents the only known fossil record of archaeocetes outside of the Eocene and comprises representatives that have a suite of primitive and derived features (Corrie & Fordyce, 2022, 2024). Providing the first description of the inner ear of Kekenodon onamata, and quantification of its shape, Corrie and Park (2024) confirm that it was capable of detecting low-frequency sounds, but not ultrasonic or infrasonic frequencies, similar to modern baleen whales. This reinforces the hypothesis that odontocetes are the only cetaceans to have evolved the capability of hearing high-frequency sounds.

The quantitative studies of inner ear morphology in cetaceans in this issue, along with the study presented by Mennecart et al. (2024) on the inner ears of fossil bovids, underscore the value of microCT for evolutionary analysis of small sensory organs. These studies demonstrate the possibility of visualising tiny morphological features in unprecedented detail. These techniques are crucial for the identification and assessment of the diagnostic traits associated with this sensory system.

Moving from the ears of mammals to those of reptiles, Werneburg and Bronzati (2024) examine the ontogeny of the reptilian ear, which, compared to the mammalian middle ear, has been somewhat neglected by comparative anatomists. The authors use histological sections of pre-cartilaginous embryonic stages to understand the formation of two key structures of the hearing apparatus of reptiles: the extracolumella, a cartilaginous structure connecting the columella (=stapes in mammals) to the tympanic membrane, and the quadrate, the site of attachment of the tympanic membrane in the skull of reptiles. Their new embryological examinations of turtles, lizards, and caimans, focusing on early blastematous stages, indicate that much of the extracolumella in turtles is derived from quadrate tissue associated with the first pharyngeal arch, whereas in lizards the dorsal portion of the extracolumella (equivalent to the dorsal columella process of caimans) similarly originate from quadrate regions. These findings challenge the uniform homology of distal columellar elements across reptiles. Integrating their results with fossil evidence, Werneburg and Bronzati (2024) propose that the ancestral columella functioned as a structural brace between quadrate and braincase. This function changed as the quadrate became integrated into jaw stress dynamics associated with novel feeding behaviours. Lastly, as anatomical observations are often subject to the researcher's individual interpretations (and assumptions), Werneburg and Bronzati (2024) stress the importance of detailed anatomical figures, including drawings and photos of histological sections, for scientific transparency.

From auditory reception to sound production, this issue features two contributions on novel sound-producing organs in birds and reptiles. Ajjim and Lang (2025) discuss crocodilian acoustic communication strategies, with a focus on gharials. Various species of crocodile, alligators and caiman have been documented using low-frequency bellows and roars, non-vocal headslaps and bubbling, as well as sub-audible vibrations for underwater communication (Senter, 2008; references therein). However, in contrast to these groups, gharials have been noted as comparatively quiet, vocalising infrequently, and their capacity to generate some of these vocal signals has been questioned, for example owing to their narrow snouts (Dinets, 2013). Here, Ajjim and Lang (2025) present novel data on the capacity of gharials (Gavialis gangeticus) to produce sudden, high amplitude pulsatile, underwater sounds. Using a combination of direct field observation and audio-video documentation, Ajjim and Lang (2025) show that these underwater sounds are tightly linked with intermittent exhalation-inhalation cycles and are only performed by adult male gharials possessing an intact ghara. The latter, a cartilaginous narial excrescence present only in males, and unique among living crocodilians. Advancing our understanding of the acoustic repertoire of gharials, Ajjim and Lang (2025) suggest that this acoustic signal represents a novel, non-vocal communication that is unique to gharial, and invite further research to unravel its behavioural significance.

Nojiri and colleagues (Nojiri et al., 2025) present novel data on the avian vocal organ, the syrinx. Among extant birds, the diversity and complexity of vocal repertoire have been coupled with the remarkable morphological diversity of the syrinx (King, 1989; Kingsley et al., 2018). The evolutionary and developmental origins of the syrinx are poorly understood, though it is thought to have arisen as a novel structure before the origin of crown birds (Clarke et al., 2016), and a recent study suggests it may have arisen through co-opting an ancient developmental program (Longtine et al., 2024). Here, Nojiri and colleagues use a comparative embryological approach to reveal the homology of the syringeal muscles. Using embryonic series from representative species belonging to the two functional classes of syrinx (Goller & Larsen, 1997; Larsen & Gollerf, 1999), those that produce sound using a single pair of vibratory membranes in the lower trachea (e.g., parrots) and those that produce sound using two pairs of vibratory tissues located at or below the tracheobronchial junction (e.g., songbirds), Nojiri et al. (2025) present three-dimensional comparisons and descriptions from serial tissue sections. The authors describe the entire morphology of the cartilage, muscles and nerves of the tracheobronchi (Nojiri et al., 2025), and provide novel evidence that the lateral tracheal muscles were ontogenetically split to form the tracheobronchial muscles and syringeal muscles in Psittaciformes (parrots) and Passeriformes (passerines). The authors hypothesise that the splitting and hypertrophy of the lateral tracheal muscles has supported the diverse acoustic strategies among birds belonging to these clades (Nojiri et al., 2025).

Lastly, departing from the mammalian auditory system itself with a novel examination of the rhythmic properties of received sounds, Laffi and colleagues (Laffi et al., 2025) present quantitative data on the motor rhythmicity of horse gaits. By using motion capture data and linear modelling to detect and characterise the different blocks of gait rhythm, comprising movement of single limbs and the pattern of interlimb coordination, Laffi et al. (2025) liken movement of the fore- and hindlimb in horses to a ticking clock. This isochronous pattern is hypothesised by the authors to reflect both physiologic and evolutionary pressures that seek to maintain coordinated motor patterns (Grillner & El Manira, 2020) and minimise energy consumption or fall risk (O'Connor et al., 2012), respectively. In demonstrating the application of bioacoustics and music cognition tools to gait kinematic analysis in the horse, Laffi et al. (2025) suggest this approach could be a viable avenue to identify gait irregularities (e.g., Weishaupt et al., 2001) and quantify locomotion in other animals.