The bony labyrinth in the temporal bone houses the sensory systems of balance and hearing. While the overall structure of the semicircular canals and cochlea is similar across therian mammals, their detailed morphology varies even among closely related groups. As such, the shape of the labyrinth carries valuable functional and phylogenetic information. Here we introduce a new, semilandmark-based three-dimensional geometric morphometric approach to shape analysis of the labyrinth, as a major improvement upon previous metric studies based on linear measurements and angles. We first provide a detailed, step-by-step description of the measurement protocol. Subsequently, we test our approach using a geographically diverse sample of 50 recent modern humans and 30 chimpanzee specimens belonging to Pan troglodytes troglodytes and P. t. verus. Our measurement protocol can be applied to CT scans of different spatial resolutions because it primarily quantifies the midline skeleton of the bony labyrinth. Accurately locating the lumen centre of the semicircular canals and the cochlea is not affected by the partial volume and thresholding effects that can make the comparison of the outer border problematic. After virtually extracting the bony labyrinth from CT scans of the temporal bone, we computed its midline skeleton by thinning the encased volume. On the resulting medial axes of the semicircular canals and cochlea we placed a sequence of semilandmarks. After Procrustes superimposition, the shape coordinates were analysed using multivariate statistics. We found statistically significant shape differences between humans and chimpanzees which corroborate previous analyses of the labyrinth based on traditional measurements. As the geometric relationship among the semilandmark coordinates was preserved throughout the analysis, we were able to quantify and visualize even small-scale shape differences. Notably, our approach made it possible to detect and visualize subtle, yet statistically significant (P = 0.009), differences between two chimpanzee subspecies in the shape of their semicircular canals. The ability to discriminate labyrinth shape at the subspecies level demonstrates that the approach presented here has great potential in future taxonomic studies of fossil specimens.
The structure and function of primate communication have attracted much attention, and vocal signals, in particular, have been studied in detail. As a general rule, larger social groups emit more types of vocal signals, including those conveying the presence of specific types of predators. The adaptive advantages of receiving and responding to alarm calls are expected to exert a selective pressure on the auditory system. Yet, the comparative biology of primate hearing is limited to select species, and little attention has been paid to the effects of social and vocal complexity on hearing. Here, we use the auditory brainstem response method to generate the largest number of standardized audiograms available for any primate radiation. We compared the auditory sensitivities of 11 strepsirrhine species with and without independent contrasts and show that social complexity explains a significant amount of variation in two audiometric parameters-overall sensitivity and high-frequency limit. We verified the generality of this latter result by augmenting our analysis with published data from nine species spanning the primate order. To account for these findings, we develop and test a model of social drive. We hypothesize that social complexity has favoured enhanced hearing sensitivities, especially at higher frequencies.
Few mammals-cetaceans, domestic cats and select bats and rodents-can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.
Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost-effective alternative-the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring-tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally-derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high-frequency limits were comparable. However, at frequencies < or =2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10-dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR- and behaviorally-derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising technique for estimating primate hearing sensitivity, but that additional data are required to explore its efficacy for estimating low-frequency thresholds.
The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.
The eponymous vocalizations of howling monkeys (genus Alouatta) are associated with territorial defense and male-male competition, yet the extreme loudness of howls, which are among the loudest vocalizations of any terrestrial mammal, have yet to be fully explained. Loudness facilitates long-distance sound propagation but the effectiveness of any vocal signal depends in part on the auditory capabilities of the intended receiver, and the auditory sensitivities of howling monkeys are unknown. To better understand the evolution of loud calls, we used the auditory brainstem response (ABR) method to estimate the auditory sensitivities of Alouatta palliata. The mean estimated audiogram of four wild-caught adults displayed a w-shaped pattern with two regions of enhanced sensitivity centered at 0.7-1.0 and 11.3 kHz. The lower-frequency region of auditory sensitivity is pitched moderately higher than the fundamental frequencies of howling, whereas the higher-frequency region corresponds well with harmonics in an infant distress call, the wrah-ha. Fitness advantages from detecting infants amid low-frequency background noise, including howling, could explain the incongruity between our ABR thresholds and the fundamental frequencies of howling. Attending to infant calls is expected to enhance reproductive success within an infanticidal genus, and we suggest that the extraordinary loudness of male howling is an indirect (runaway) result of positive feedback between the selective pressures of hearing infant distress calls and deterring infanticide.
New World monkeys are a diverse primate group and a model for understanding hearing in mammals. However, comparable audiograms do not exist for the larger monkeys, making it difficult to test the hypothesized relationship between interaural distance and high-frequency hearing limit (i.e., the allometric model). Here, the auditory brainstem response (ABR) method is used to assess auditory sensitivity in four tufted capuchins (Sapajus apella), a large monkey with a large interaural distance. A primate-typical four-peak pattern in the ABR waveforms was found with peak latencies from ca. 2 to 12 ms after stimulus onset. Response amplitude decreased linearly with decreasing stimulus level (mean r = 0.93, standard deviation 0.14). Individual variation in each threshold was moderate (mean ± 7 dB). The 10-dB bandwidth of enhanced sensitivity was 2-16 kHz-a range comparable to smaller monkeys and congruent with the bandwidth of their vocal repertoire. In accord with the general principles of the allometric model, the 60-dB high-frequency limit of S. apella (26 kHz) is lower than those of smaller-headed monkeys; however, it is substantially lower than 44.7 kHz, the value predicted by the allometric model. These findings and other exceptions to the allometric model warrant cautious application and further investigation of other potential selective factors.
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