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Bony labyrinths and mastoid cavities of Heterocephalus. WinSurf reconstructions of the left bony labyrinths and mastoid cavities of three Heterocephalus specimens of different ages, seen from approximately posterior views. In the youngest specimen on the left, coloured arrows indicate the future directions of expansion of the middle ear cavity into the mastoid region. Blue = dorsal mastoid cavity; green = ventral mastoid cavity; orange = posteromedial mastoid cavity. The 38-month-old specimen had smaller mastoid cavities than many younger specimens, so this diagram should not be taken to indicate a strict temporal sequence. APSC = ampulla for posterior semicircular canal; ASC = anterior semicircular canal; C = cochlea; DMC = dorsal mastoid cavity; ED = bony tube for endolymphatic duct; ER = epitympanic recess; FP = footplate of stapes; HM = head of malleus; LA = lenticular apophysis of incus; LPI = long process of incus; LSC = lateral semicircular canal; MI = malleoincus; MM = manubrium of malleus; OW = oval window; PC = posterior crus of stapes; PD = bony tube for perilymphatic duct (canaliculus cochleae); PMC = posteromedial mastoid cavity; PSC = posterior semicircular canal; RW = round window; SPI = short process of incus; TC = tympanic cavity; TM = tympanic membrane; TT = tensor tympani tendon; V = vestibule of inner ear; VMC = ventral mastoid cavity. doi:10.1371/journal.pone.0167079.g006
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Although increasingly popular as a laboratory species, very little is known about the peripheral auditory system of the naked mole-rat, Heterocephalus glaber. In this study, middle and inner ears of naked mole-rats of a range of ages were examined using micro-computed tomography and dissection. The ears of five other bathyergid species (Bathyergus...
Citations
... African mole-rats (Bathyergidae), a family of strictly subterranean rodent species distributed throughout sub-Saharan Africa, have long been the focus of comparative research on the adaptations of mammalian sensory systems to life underground Vice et al., 2021). Arguably, their most extensively examined sensory modality is hearing, which has been well characterized in the cooperatively-breeding genera Fukomys (Northern common mole-rats - Müller et al., 1992;Kössl et al., 1996;Brückmann and Burda, 1997;Lange, 2006;Gerhardt et al., 2017;Pyott et al., 2020;Caspar et al., 2021) and Heterocephalus (naked mole-rat - Heffner and Heffner, 1993;Mason et al., 2016;Okanoya et al., 2018;Pyott et al., 2020). ...
... This unusual condition was also remarked upon by Burda et al. (1992) and deemed typical for subterranean mammals. Furthermore, Mason et al. (2016) reported a narrow and semi-occluded external meatus for H. glaber, with a length of 6 mm and a diameter of 0.6 mm, and suggested that this reduces the sound energy reaching the tympanic membrane. Our micro CT data supports these previous reports of a generally narrow and elongated meatus, while revealing species-specific variations in its shape (Figs 1, S1). ...
African mole-rats display highly derived hearing that is characterized by low sensitivity and a narrow auditory range restricted to low frequencies < 10 kHz. Recently, it has been suggested that two species of these rodents do not exhibit distortion product otoacoustic emissions (DPOAE), which was interpreted as evidence for a lack of cochlear amplification. If true, this would make them unique among mammals. However, both theoretical considerations on the generation of DPOAE as well as previously published experimental evidence challenge this assumption. We measured DPOAE and stimulus-frequency otoacoustic emissions (SFOAE) in three species of African mole-rats (Ansell's mole-rat-Fukomys anselli; Mashona mole-rat-Fukomys darlingi; naked mole-rat-Heterocephalus glaber) and found unexceptional otoacoustic emission values. Measurements were complicated by the remarkably long, narrow and curved external ear canals of these animals, for which we provide a morphological description. Both DPOAE and SFOAE displayed the highest amplitudes near 1 kHz, which corresponds to the region of best hearing in all tested species as well as to the frequency region of the low-frequency acoustic fovea previously described in Ansell's mole-rat. Thus, the cochlea in African mole-rats shares the ability to generate evoked otoacoustic emission with other mammals.
... Naked mole rats (Heterocephalus glaber), a subterranean-dwelling species native to eastern equatorial Africa, have an extraordinarily long maximal lifespan-31 years (Ruby et al., 2018) -and remarkable resistance to cancer and other age-related pathologies (Oka et al., 2023). Although their hearing thresholds are notably elevated compared other (non-subterranean) rodents even at young ages (Heffner and Heffner, 1993;Pyott et al., 2020), the morphology of the middle and inner ear (Mason et al., 2016) and the organization of the cochlear sensorineural structures into inner and outer hair cells (Barone et al., 2019) share similarities with other rodents and humans. Thus, naked mole rats provide a unique system to examine age-related changes in the cochlea in an otherwise disease-free context. ...
... Analyzed individuals included both males and females, mostly of unknown age. Although the development of caviomorph inner ears was not separately studied, age does not seem to appreciably affect inner ear morphology in Phiomorpha (e.g., Fukomys, Lindenlaub and Burda 1993;Heterocephalus, Mason et al. 2016), nor mammals in general (e.g., Hoyte 1961;Jeffery and Spoor 2004;Ekdale 2013;Mason et al. 2016;Mennecart and Costeur 2016;Thean et al. 2017; but see Sánchez-Villagra and Schmelzle 2007). Regarding fossil taxa, our sample includes a total of eleven different extinct species from the West Indies (N = 12 specimens) and South American mainland (N = 1 specimen). ...
With their past and current diversities, West Indian caviomorph rodents dominate the terrestrial mammalian fauna of the Caribbean archipelago. Many of these species have recently become extinct, including the emblematic giant forms known as Heptaxodontidae. The higher-level systematics and content of this family have been widely disputed over the last decades (i.e., membership in Cavioidea vs. Chinchilloidea vs. Octodontoidea). Here we analyzed the phylogenetic signal provided by several characters of the caviomorph inner ear to adress the phylogenetic affinities of the West Indian heptaxodontids. For this, we assembled an exhaustive taxonomic sampling (N = 100) of extant North and South American caviomorphs (including representatives of all families) and a wide array of West Indian forms among octodontoid echimyids (extant and extinct capromyines, as well as extinct heteropsomyines), and some heptaxodontid subfossil taxa such as Amblyrhiza, Clidomys, and Elasmodontomys. Geometric morphometrics and comparative phylogenetic methods were employed to explore shape differences of the inner ear and their potential systematic implications. Our results show that: (1) allometry is a major contributor to shape variation in the bony labyrinth; (2) shape variation bears a strong phylogenetic signal, providing diagnostic characters for Caviidae and Erethizontoidea; and (3) Amblyrhiza and Clidomys are morphologically closer to Chinchilloidea with which they have potential phylogenetic affinities. Elasmodontomys remains a problematic taxon as it exhibits inner ear features that are consistent with either Chinchilloidea or Octodontoidea, depending on how the allometric component is evaluated.
... Most subterranean taxa had very large semicircular canals, yielding increased sensitivity to head rotations in all directions (McVean, 1999;Muller, 1999;Pfaff et al 2015). Additionally, subterranean taxa were characterised by a very long cochlea with many turns, leading to a high sensitivity to lowfrequency sounds, which attenuate less rapidly in underground environments (Lange et al. 2004;Ekdale 2013;Crumpton et al. 2015;Mason et al. 2016). Finally, agile species that pursue moving prey evolved very large semicircular canals, conferring increased sensitivity to head rotations in all directions, which is necessary for fast movements and good reflexes with respect to posture, balance and eye movements (Muller, 1999;Spoor et al. 2007). ...
Evolutionary convergence in distantly related species is among the most convincing evidence of adaptive evolution. The mammalian ear, responsible for balance and hearing, is not only characterised by its spectacular evolutionary incorporation of several bones of the jaw, it also varies considerably in shape across modern mammals. Using a new multivariate approach, we show that in Afrotheria, a monophyletic clade with morphologically and ecologically highly disparate species, inner ear shape evolved similar adaptations as in non-afrotherian mammals. We identified four trait combinations that underlie this convergence. The high evolvability of the mammalian ear is surprising: nowhere else in the skeleton are different functional units so close together; it includes the smallest bones of the skeleton, and is encapsulated within the densest bone. We suggest that this evolvability is a direct consequence of the increased genetic and developmental complexity of the mammalian ear compared to other vertebrates.
... Its excellent low-frequency hearing is associated with an expanded middle ear cavity (Ravicz & Rosowski, 1997), a feature commonly found in small mammals from arid regions (Mason, 2016a,b). The middle ear cavity of the naked mole-rat, however, is much less voluminous (Mason, Cornwall & Smith, 2016). ...
... Several aspects of naked mole-rat ear morphology are indicative of reduced functionality and may contribute to these limitations (Mason et al., 2016). Recent work showed that these animals have missing or abnormally organised hair Clarifying the myths of naked mole-rat biology bundles on their cochlear outer hair cells (Pyott et al., 2020). ...
Naked mole-rats (NMRs, Heterocephalus glaber) are the longest-lived rodents with a maximum life span exceeding 37 years. They exhibit a delayed aging phenotype and resistance to age-related functional decline/diseases. Specifically, they do not display increased mortality with age, maintain several physiological functions until nearly the end of their lifetime, and rarely develop cancer and Alzheimer's disease. NMRs live in a hypoxic environment in underground colonies in East Africa and are highly tolerant of hypoxia. These unique characteristics of NMRs have attracted considerable interest from zoological and biomedical researchers. This review summarizes previous studies of the ecology, hypoxia tolerance, longevity/delayed aging, and cancer resistance of NMRs and discusses possible mechanisms contributing to their healthy aging. In addition, we discuss current issues and future perspectives to fully elucidate the mechanisms underlying delayed aging and resistance to age-related diseases in NMRs.
Expected final online publication date for the Annual Review of Animal Biosciences, Volume 11 is February 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... The comparative anatomical evidence that is currently available is inconclusive in this regard. The southern marsupial mole (Notoryctes typhlops) has wider SCCs than non-subterranean marsupials (Pfaff et al. 2017); bathyergid mole rats were reported to have unusually wide SCCs (Mason et al. 2016); Cryptomys sp. and blind mole rats have SCCs that are, relative to body mass, longer and have a wider internal diameter and a larger radius of curvature than brown rats (Rattus norvegicus) (Lindenlaub et al. 1995); the European mole (Talpa europaea) also has (absolutely) longer and wider SCCs than brown rats (McVean 1999); the greater mole rat (Spalax microphthalmos) and the southern marsupial mole have wider SCCs than aerial and arboreal members of the squirrel-related clade, while the European mole has not (Pfaff et al. 2015); and, finally, subterranean mammals belonging to the Chrysochloridae, Talpidae, Tenrecidae, and Marsupialia were not consistently found to have enlarged semicircular canals compared with non-subterranean species (Crumpton et al. 2015). Although a high internal diameter of the SCCs (wide canals) is a recurring observation, these reports typically lack phylogenetically informed statistics (Lindenlaub et al. 1995;McVean 1999;Crumpton et al. 2015;Mason et al. 2016), and those studies that do include evolutionary history in their analyses show a moderate to strong phylogenetic signal (Pagel's lambda close to one; Pfaff et al. 2015Pfaff et al. , 2017. ...
... The southern marsupial mole (Notoryctes typhlops) has wider SCCs than non-subterranean marsupials (Pfaff et al. 2017); bathyergid mole rats were reported to have unusually wide SCCs (Mason et al. 2016); Cryptomys sp. and blind mole rats have SCCs that are, relative to body mass, longer and have a wider internal diameter and a larger radius of curvature than brown rats (Rattus norvegicus) (Lindenlaub et al. 1995); the European mole (Talpa europaea) also has (absolutely) longer and wider SCCs than brown rats (McVean 1999); the greater mole rat (Spalax microphthalmos) and the southern marsupial mole have wider SCCs than aerial and arboreal members of the squirrel-related clade, while the European mole has not (Pfaff et al. 2015); and, finally, subterranean mammals belonging to the Chrysochloridae, Talpidae, Tenrecidae, and Marsupialia were not consistently found to have enlarged semicircular canals compared with non-subterranean species (Crumpton et al. 2015). Although a high internal diameter of the SCCs (wide canals) is a recurring observation, these reports typically lack phylogenetically informed statistics (Lindenlaub et al. 1995;McVean 1999;Crumpton et al. 2015;Mason et al. 2016), and those studies that do include evolutionary history in their analyses show a moderate to strong phylogenetic signal (Pagel's lambda close to one; Pfaff et al. 2015Pfaff et al. , 2017. The studies that estimated SCC sensitivity using simple equations found that Cryptomys sp. ...
... In addition to the aforementioned five specimens, we used CT scans of the ear regions of a further four adult or near-adult naked mole rats from the same colony (aged between 4 and 65 months old), which had been made as part of a previous study (Mason et al. 2016). Heads of three specimens from a different colony, stained with iodine, had been obtained from Dr Phil Cox: one ear region from each of these mole rats were also scanned, as was the ear region of one laboratory mouse (Mus musculus) and the whole head of a second mouse. ...
The vertebrate vestibular system is crucial for balance and navigation, and the evolution of its form and function in relation to species' lifestyle and mode of locomotion has been the focus of considerable recent study. Most research, however, has concentrated on aboveground mammals, with much less published on subterranean fauna. Here, we explored variation in anatomy and sensitivity of the semicircular canals among 91 mammal species, including both subterranean and non-subterranean representatives. Quantitative phylogenetically informed analyses showed significant widening of the canals relative to radius of curvature in subterranean species. A relative canal width above 0.166 indicates with 95% certainty that a species is subterranean. Fluid-structure interaction modelling predicted that canal widening leads to a substantial increase in canal sensitivity; a reasonably good estimation of the absolute sensitivity is possible based on the absolute internal canal width alone. In addition, phylogenetic comparative modelling and functional landscape exploration revealed repeated independent evolution of increased relative canal width and anterior canal sensitivity associated with the transition to a subterranean lifestyle, providing evidence of parallel adaptation. Our results suggest that living in dark, subterranean tunnels requires good balance and/or navigation skills which may be facilitated by more sensitive semicircular canals.
... Other ruminants we found as cited sources point to the cow (Costeur et al. 2016), sheep (Simaei et al. 2017;Péus et al. 2020), and buffalo (Nourinezhad et al. 2021), where the anatomical description of the ossicles is available in the same general manner. In studies published for other species (the naked mole-rat, Guinea pig, paca, and chinchilla), the authors mention a maleo-incal complex, resulted from the fusion of the maleus and incus in a single piece (Martins et al. 2015;Mason et al. 2016;Guan et al. 2019;Martonos et al. 2019). ...
The study provides a series of distinctive morphological features of the auditory ossicles alongside comparative morphometric data, bringing facts in respect to morphology and some morpho-functional elements of the auditory ossicles in this little-studied species. The most relevant features noted are evident conical shape of muscular process of malleus and triangular aspect of the handle of malleus. For the incus, a short body of the bone and the direct continuation is mentioned, with no clear distinction as an individualized piece for the lenticular process. As for the stapes, the clear profiling of the muscular tubercle for the stapedial muscle and elliptic shape of the foot of the stapes is noted. A series of comparative measurements and indices are also calculated in the attempt of profiling differences from the domestic couterspecies- sheep and goat.
... However, pinnae in rodents were shown to be responsible for acoustical gain at frequencies above 8 kHz, therefore the missing pinnae could not account for the elevated auditory thresholds at low frequency (Koka et al., 2011;Lauer et al., 2011). Furthermore, in NMR findings from microcomputed tomography also suggest that the gross dimensions of the middle and inner ear may not be sufficient to explain altered hearing (Mason et al., 2016). Based on well-curated hearing genotype-phenotype database, amino acid substitutions that matches pathogenic mutations in humans in the hair bundle link proteins were identified in DMR. ...
Evolutionary medicine has been a fast-growing field of biological research in the past decade. One of the strengths of evolutionary medicine is to use non-traditional model organisms which often exhibit unusual characteristics shaped by natural selection. Studying these unusual traits could provide valuable insight to understand biomedical questions, since natural selection likely discovers solutions to those complex biological problems. Because of many unusual traits, the naked mole-rat (NMR) has attracted attention from different research areas such as aging, cancer, and hypoxia- and hypercapnia-related disorders. However, such uniqueness of NMR physiology may sometimes make the translational study to human research difficult. Damaraland mole-rat (DMR) shares multiple characteristics in common with NMR, but shows higher degree of similarity with human in some aspects of their physiology. Research on DMR could therefore offer alternative insights and might bridge the gap between experimental findings from NMR to human biomedical research. In this review, we discuss studies of DMR as an extension of the current set of model organisms to help better understand different aspects of human biology and disease. We hope to encourage researchers to consider studying DMR together with NMR. By studying these two similar but evolutionarily distinct species, we can harvest the power of convergent evolution and avoid the potential biased conclusions based on life-history of a single species.
... Although the ecology, physiology, and behavior of bathyergids are well-documented 19,29 , their appendicular adaptations have been surprisingly ignored. Most of the studies of their skeleton have focused on cranial features [30][31][32] . Similarly, their fossil record is largely represented by cranial and dental material 28 , so that little is known about their appendicular skeleton. ...
Life underground has constrained the evolution of subterranean mammals to maximize digging performance. However, the mechanisms modulating morphological change and development of fossorial adaptations in such taxa are still poorly known. We assessed the morpho-functional diversity and early postnatal development of fossorial adaptations (bone superstructures) in the appendicular system of the African mole-rats (Bathyergidae), a highly specialized subterranean rodent family. Although bathyergids can use claws or incisors for digging, all genera presented highly specialized bone superstructures associated with scratch-digging behavior. Surprisingly, Heterocephalus glaber differed substantially from other bathyergids, and from fossorial mammals by possessing a less specialized humerus, tibia and fibula. Our data suggest strong functional and developmental constraints driving the selection of limb specializations in most bathyergids, but more relaxed pressures acting on the limbs of H. glaber. A combination of historical, developmental and ecological factors in Heterocephalus are hypothesized to have played important roles in shaping its appendicular phenotype. Morphological and developmental analyses demonstrated that the naked mole-rats are the least anatomically specialized bathyergid for scratch-digging. Developmental, ecological and historical factors may be involved in such peculiar phenotype
... The cristae to subdivide the quadrate diverticulum have not been paid attention to in archosaurs previously. Although their presence might be purely for structural purpose, in some mammals, the middle ear space is divided into sub-cavities with septa or partial septa (e.g., Argyle & Mason, 2008;Mason, 2016;Mason et al., 2016). Mason et al. (2016) discussed the resonance effects of the divisions by septa in mammals given that more resonance impact has been observed in cavities with less septa compared to smaller sub-cavities with more septa, in addition to the structural purpose of the septa. ...
... Although their presence might be purely for structural purpose, in some mammals, the middle ear space is divided into sub-cavities with septa or partial septa (e.g., Argyle & Mason, 2008;Mason, 2016;Mason et al., 2016). Mason et al. (2016) discussed the resonance effects of the divisions by septa in mammals given that more resonance impact has been observed in cavities with less septa compared to smaller sub-cavities with more septa, in addition to the structural purpose of the septa. Thus, we cannot rule out potential resonance function of the septa for the quadrate diverticulum in alligator, and this might be of interest for the future research of hearing capability of alligator. ...
Crocodylia has an extensive epithelial pneumatic space in the middle ear, paratympanic sinus system. Although fossil and extant crocodylian paratympanic sinus systems have been studied recently using the computed tomography (CT) and three‐dimensional (3D) reconstruction data, due to the soft tissue nature of the pneumatic system and presence of its surrounding soft tissue structures, some boundaries, and definitions of each extension remain ambiguous. We describe the comprehensive paratympanic sinus system in posthatched alligator using soft tissue enhanced CT data with 3D reconstructions. The data are compared to the available data to discuss the ontogenetic pattern in alligator. We introduce further divided entities of the pneumatic system based on their associated bony and soft tissue structures and epithelial membrane and clarify the pneumatic terminologies. We then re‐visit the potential homology of the paratympanic sinus in Archosauria. Epithelial boundaries of the ventral portion of the pneumatic system from the histological data suggest that the dual origin of the basioccipital diverticulum derived from the tympanic sinus and basicranial diverticulum medially. The presence of the epithelial boundary and pneumatic changes in ontogeny suggests that the middle ear may function differently in developmental stages. Lastly, a morphogenetic tree is constructed to help future work of comparative developmental studies of the paratympanic sinus system between crocodiles and birds.
