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 (Burda et al., 1992; 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).

The underground tunnel systems inhabited by these animals represent a special acoustic environment: frequencies above 1 kHz are strongly attenuated over distances of just a few meters, while lower frequencies may experience a sound pressure amplification of more than 6 dB per meter (Heth et al., 1986; Lange et al., 2007; Okanoya et al., 2018). This phenomenon, known as the ‘stethoscope effect’, likely had a major impact on the evolution of the auditory system in subterranean mammals. The hearing range of some African mole-rats and other geologically old lineages (> 20 million years old) of burrowing rodents is conspicuously narrow and restricted (at 60 dB SPL) to low frequencies between 20 Hz and 6 kHz (Heffner and Heffner, 1990, 1992, 1993). Indeed, they display “the most restricted high-frequency hearing yet observed among mammals” (Heffner and Heffner, 1992; see also Gerhardt et al., 2017). Reflecting the acoustic properties of their tunnels, auditory sensitivity is greatest at frequencies around 1 kHz, although hearing thresholds in this frequency range are still 30 – 40 dB SPL - much higher than those of most surface-dwelling rodents (Gerhardt et al., 2017; Caspar et al., 2021). Furthermore, behavioural studies suggest a loss of directional hearing in bathyergids, as indicated by the inability of naked mole-rats to localize short sound bursts (Heffner and Heffner, 1993).

While mole-rat hearing capabilities appear poor in comparison to other rodents, the rich vocal repertoire of common and naked mole-rats suggests that the auditory sense is nonetheless highly relevant (Dvořáková et al., 2016; Barker et al., 2021). This view is supported by interesting specializations of the inner ear: Müller et al. (1992) described a cochlear place-frequency map for Ansell's mole-rat (Fukomys anselli), indicating the presence of an acoustic fovea at low frequencies (note that the 20th century literature refers to this species as Cryptomys hottentotus, since it was only formally described in 1999; see Begall et al., 2021 for a complete synonymy). Müller et al. (1992) found that the frequencies between approximately 0.6 and 1.0 kHz occupied more than 5 mm of the total length of the basilar membrane (12.9 mm), whereas all other frequency ranges occupied less than 1 mm per octave. Differing from the acoustic foveae of bats (e.g., Kössl and Vater, 1995), but similar to that of the barn owl (Tyto alba - Köppl et al., 1993), frequency selectivity in the foveal region of Ansell's mole-rat is not unusually high (Kössl et al., 1996). Whether similar acoustic foveae are present in other African mole-rats remains to be demonstrated, but great morphological similarities of the organ of Corti across the sister genera Fukomys and Cryptomys (Southern common mole-rats) suggests that this might indeed be the case (Lange, 2006). Recently, Pyott et al. (2020) suggested that another peculiarity should be added to the unusual auditory characteristics of African mole-rats: the absence of otoacoustic emissions (OAE).

OAE are sounds that are generated in the cochlea and emitted from the ear. Such otoacoustic emissions are in general emitted in response to external stimuli and are indicators for active amplification processes in the hair cells of the organ of Corti that under normal circumstances support the perception of low-level sounds and, as such, are also indicators of a healthy cochlea. Human ears commonly emit a spectrum of spontaneous otoacoustic emissions (SOAE), and the frequency selectivity of their suppression has been used to estimate cochlear tuning (Manley and van Dijk, 2016). SOAE are most frequent in young people and are gradually lost with age (Abada et al., 2017), which suggests that damage to hair cells or cochlear defects are not a cause of SOAE. SOAE have also been reported from rodents, including certain mutant laboratory mice strains (Cheatham et al., 2016) and caviomorphs (chinchillas - Clark et al., 1984; guinea pigs - Ohyama et al., 1991). The latter are closely related to African mole-rats within the hystricomorph rodent radiation.

Since OAE can be influenced by externally added sounds, they are attractive as a window into cochlear function and thus of interest for clinical diagnosis. SOAE only occur idiosyncratically at certain frequencies and become less common with increasing age, so are not generally suitable as a diagnostic tool. Instead, click-evoked OAE or OAE evoked using two tones are more commonly studied. Distortion-product OAE (DPOAE) arise when two tones are simultaneously processed by the same hair cells (Barral and Martin, 2012). DPOAE have been extensively studied in a range of tetrapod species and new data can thus be compared to a large interspecific database (e.g., amphibians, Van Dijk and Manley, 2001; lizards, Manley et al., 1993; birds, Taschenberger and Manley, 1998; and mammals, Martin et al., 1987, including humans, Reuters and Hammershøi, 2006). More recently, so-called stimulus-frequency OAE (SFOAE) have received more interest, since they are evoked by single tones (Shera and Guinan, 2003). These are then suppressed by an added nearby tone, and the suppressed portion of the signal indicates the active component that is measured.

So far, two studies on African mole-rats have aimed to measure OAE. Initially, Kössl et al. (1996) detected robust DPOAE in Ansell's mole-rat. More recently, however, Pyott et al. (2020) reported the absence of DPOAE in naked mole-rats and Damaraland mole-rats (Fukomys damarensis), while by contrast they were able to measure DPOAE in mice. The authors concluded that these bathyergids are unique among mammals in lacking cochlear amplification, which could be the cause for their decreased hearing sensitivity (Pyott et al., 2020). They found that while prestin is expressed in the outer hair cells of mole-rats, the outer hair cell stereocilial bundles, which are crucial for enabling cochlear amplification, displayed a distorted morphology or were even absent in apical regions of the cochlea (Pyott et al., 2020). As Pyott et al. (2020) and Kössl et al. (1996) used different species of bathyergids, it is currently unclear whether the absence of OAE is a species-specific phenomenon or may point to methodological issues with the experimental procedures that Pyott et al. (2020) employed (Caspar et al., 2021). To address this question, we here measured OAE in three species of bathyergids, including the Ansell's mole-rat used by Kössl et al. (1996) and the naked mole-rat used by Pyott et al. (2020). As expected from general physiological considerations, we were able to measure emissions in all three species.