Evolution of the auditory ossicles in extant hominids: metric variation in African apes and humans.

The auditory ossicles in primates have proven to be a reliable source of phylogenetic information. Nevertheless, to date, very little data have been published on the metric dimensions of the ear ossicles in African apes and humans. The present study relies on the largest samples of African ape ear ossicles studied to date to address questions of taxonomic differences and the evolutionary transformation of the ossicles in gorillas, chimpanzees and humans. Both African ape taxa show a malleus that is characterized by a long and slender manubrium and relatively short corpus, whereas humans show the opposite constellation of a short and thick manubrium and relatively long corpus. These changes in the manubrium are plausibly linked with changes in the size of the tympanic membrane. The main difference between the incus in African apes and humans seems to be related to changes in the functional length. Compared with chimpanzees, human incudes are larger in nearly all dimensions, except articular facet height, and show a more open angle between the axes. The gorilla incus resembles humans more closely in its metric dimensions, including functional length, perhaps as a result of the dramatically larger body size compared with chimpanzees. The differences between the stapedes of humans and African apes are primarily size-related, with humans being larger in nearly all dimensions. Nevertheless, some distinctions between the African apes were found in the obturator foramen and head height. Although correlations between metric variables in different ossicles were generally lower than those between variables in the same bone, variables of the malleus/incus complex appear to be more strongly correlated than those of the incus/stapes complex, perhaps reflecting the different embryological and evolutionary origins of the ossicles. The middle ear lever ratio for the African apes is similar to other haplorhines, but humans show the lowest lever ratio within primates. Very low levels of sexual dimorphism were found in the ossicles within each taxon, but some relationship with body size and several dimensions of the ear bones was found. Several of the metric distinctions in the incus and stapes imply a slightly different articulation of the ossicular chain within the tympanic cavity in African apes compared with humans. The limited auditory implications of these metric differences in the ossicles are also discussed. Finally, the results of this study suggest that several plesiomorphic features for apes may be retained in the ear bones of the early hominin taxa Australopithecus and Paranthropus as well as in the Neandertals.

Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing.

Mammals are unique in being the only group of amniotes that can hear sounds in the upper frequency range (>12 kHz), yet details about the evolutionary development of hearing patterns remain poorly understood. In this study, we used high resolution X-ray computed tomography to investigate several functionally relevant auditory structures of the inner ear in a sample of 21 fossil primate species (60 Ma to recent times) and 25 species of living euarchontans (primates, tree shrews, and flying lemurs). The structures examined include the length of the cochlea, development of bony spiral lamina and area of the oval window (or stapedial footplate when present). Using these measurements we predicted aspects of low-frequency and high-frequency sensitivity and show that hearing patterns in primates likely evolved in several stages through the first half of the Cenozoic. These results provide temporal boundaries for the development of hearing patterns in extant lineages and strongly suggest that the ancestral euarchontan hearing pattern was characterized by good high-frequency hearing but relatively poor low-frequency sensitivity. They also show that haplorhines are unique among primates (extant or extinct) in having relatively longer cochleae and increased low-frequency sensitivity. We combined these results with additional, older paleontological evidence to put these findings in a broader evolutionary context.

Relationships between the expression of the stapedial artery and the size of the obturator foramen in euarchontans: Functional and phylogenetic implications.

Cranial arterial patterns are commonly used for determining phylogenetic patterns in extant taxa and have often been used in studies investigating the relationships among fossil taxa. In primitive eutherians, the stapedial artery provided blood to the meninges, orbits, and certain regions of the face. In many modern mammals, however, blood supply to most of these areas has been taken over by branches of the external carotid, although some groups (e.g., treeshrews, some families of primates) still retain aspects of the ancestral pattern. Here, we show that the relative size of the obturator foramen of the stapes is a reliable indicator of the presence or absence of a "functional" stapedial artery in Euarchonta. We also describe newly discovered stapedes for extinct euarchontans, Ignacius graybullianus, and Plesiadapis tricuspidens, and use the approach described here to show that these taxa likely did not have a functional stapedial artery. The implications of these findings for auditory function and phylogenetic studies are discussed.

Auditory morphology and hearing sensitivity in fossil New World monkeys.

In recent years it has become possible to investigate the hearing capabilities in fossils by analogy with studies in living taxa that correlate the bony morphology of the auditory system with hearing sensitivity. In this analysis, we used a jack-knife procedure to test the accuracy of one such study that examined the functional morphology of the primate auditory system and we found that low-frequency hearing (sound pressure level at 250 Hz) can be predicted with relatively high confidence (±3-8 dB depending on the structure). Based on these functional relationships, we then used high-resolution computed tomography to examine the auditory region of three fossil New World monkeys (Homunculus, Dolicocebus, and Tremacebus) and compared their morphology and predicted low-frequency sensitivity with a phylogenetically diverse sample of extant primates. These comparisons reveal that these extinct taxa shared many auditory characteristics with living platyrrhines. However, the fossil with the best preserved auditory region (Homunculus) also displayed a few unique features such as the relative size of the tympanic membrane and stapedial footplate and the degree of trabeculation of the anterior accessory cavity. Still, the majority of evidence suggests that these fossil species likely had similar low-frequency sensitivity to extant South American monkeys. This research adds to the small but growing body of evidence on the evolution of hearing abilities in extinct taxa and lays the groundwork for predicting hearing sensitivity in additional fossil primate specimens.

Correlations between auditory structures and hearing sensitivity in non-human primates.

Primates show distinctions in hearing sensitivity and auditory morphology that generally follow phylogenetic patterns. However, few previous studies have attempted to investigate how differences in primate hearing are directly related to differences in ear morphology. This research helps fill this void by exploring the form-to-function relationships of the auditory system in a phylogenetically broad sample of non-human primates. Numerous structures from the outer, middle, and inner ears were measured in taxa with known hearing capabilities. The structures investigated include the overall size and shape of the pinna, the areas of the tympanic membrane and stapedial footplate, the masses and lever arm lengths of the ossicles, the volumes of the middle ear cavities, and the length of the cochlea. The results demonstrate that a variety of auditory structures show significant correlations with certain aspects of hearing (particularly low-frequency sensitivity). Although the majority of these relationships agree with expectations from auditory theory, some traditional (and possibly outdated) ideas were not supported. For example, the common misconception that higher middle ear transformer ratios (e.g., impedance transformer ratio) result in increased hearing sensitivity was not supported. Although simple correlations between form and function do not necessarily imply causality, the relationships defined in this study not only increase our understanding of auditory patterns in extant taxa but also lay the foundation to begin investigating the hearing in fossil primates.

What does geometric mean, mean geometrically? Assessing the utility of geometric mean and other size variables in studies of skull allometry.

This study investigated the effects of using different size variables for interpretations of relative orbit size and mandibular robusticity. Thirty-three skull measurements taken on 385 platyrrhines representing 12 of 16 New World monkey genera (in addition to body mass and total body length) were used singly and in combinations (by taking the geometric mean of all measurements) as size variables to produce relative size indices of orbit area and mandibular thickness. These indices were then compared to investigate which size variables proved effective at differentiating nocturnal from diurnal taxa and hard object from soft object feeders based upon results from previous biomechanical studies. It was found that certain groups of size variables consistently produced the a priori expectations and resulted in lower coefficients of variation. The general principles shared by these size variables were that they sampled anatomically remote regions of the skull that appear to be functionally independent from the trait being evaluated and they were nearly always geometric mean combinations composed of a relatively high number (>or=12) of large measurements. Suggestions are also presented for amending these principles for use with incomplete material such as fossils.

Primate auditory diversity and its influence on hearing performance.

The auditory region contains numerous structures that have proven useful for phylogenetic classification at various taxonomic levels. However, little work has been done in primates relating differences in morphology to variations in hearing performance. This study documents anatomical and physiological distinctions within primates and begins to address the functional and evolutionary consequences of these and other auditory features. The dimensions of the outer ear (pinna) were measured in cadaveric specimens representing nearly every primate family and used to calculate a shape ratio (height/width). It was found that nonanthropoids have a significantly higher ratio than anthropoids, although the actual height was not found to differ. This indicates that most nonanthropoids have ears that are tall and narrow, whereas monkeys and apes are characterized by ears with more equal height and width dimensions. Eardrum area, stapedial footplate area, and ossicular lever arm lengths were measured in dried specimens to calculate an impedance transformer ratio. A distinction was found between anthropoids and strepsirrhines, with the latter group having a transformer ratio indicative of a higher percentage of acoustic energy transmission through the middle ear. Audiogram data were gathered from the literature to analyze hearing sensitivity and it was found that platyrrhines illustrate more low-frequency sensitivity than like-sized lorisoids. The effects of intraspecific variation on the audiogram results were also examined and were found to produce similar results as the analysis using species mean threshold values. Lastly, correlations between morphological and audiogram variables were examined. Several measures of hearing sensitivity were found to be correlated with pinna shape but correlations with middle ear transmission properties were weaker. In addition to using traditional statistical techniques, phylogenetic corrective methods were applied to address the problem of statistical nonindependence of the data and the results of both analyses are compared. These findings are discussed with respect to how sensory adaptations and phylogenetic history may be related to the current radiation of primates.