Descent of the hyoid in chimpanzees: evolution of face flattening and speech
Introduction
The evolution of human speech has attracted much interest to better understand the evolution of language. Human speech has the distinct feature that humans can regularly utter several phonemes—including vowels and consonants—sequentially and rapidly in a short, single exhalation. It must be noted that speech per se is not the same as language and does not necessarily reflect the high intelligence of humans. However, this sophisticated feature of speech allows humans to turn much information that is encoded by language in the brain into sounds and to communicate it to others rapidly and efficiently (P. Lieberman, 1984). Therefore, even if language and speech arose independently in the human lineage, an understanding of the evolution of speech would shed light on the evolution of language with which we are endowed today.
Theories of speech physiology and acoustics demonstrate that humans have a unique anatomy of the supralaryngeal vocal tract (SVT) that underlies its sophisticated manipulation in the production of speech. Humans and nonhuman mammals basically make use of the same machinery for speech and vocalization: the lungs generate sound power, the vocal folds in the larynx comprise the sound sources, and the SVT resonates the sources to generate voiced sounds with some bands of the formant frequencies, e.g., vowels in speech (Fant, 1960, Lieberman and Blumstein, 1988, Titze, 1994, Stevens, 1998, Fitch and Hauser, 2003, Riede et al., 2005). The distribution pattern of the formants defines the different kinds of vowels that form the platform for vocal communication. These are determined by the resonance properties of the SVT and these properties in turn are dictated by the volumetric topology of the tract, which can be estimated from a function of the sequential cross-sectional area along the tract. The SVT in most mammals, including humans, is principally composed of two cavities: the horizontal oral and vertical pharyngeal cavities designated here the SVTH and SVTV, respectively. In nonhuman mammals, the SVTV is much shorter than the SVTH (Negus, 1949, Lieberman, 1984, Laitman and Reidenberg, 1993, Dyce et al., 1996). Their epiglottis, which is attached to the thyroid cartilage of the laryngeal skeleton, maintains contact with the velum and prevents the SVTV from facing the movable tongue. The tongue is also long in the horizontal direction, fitting this configuration. Although this anatomy allows the oral cavity to function as a single resonator, it prevents the pharyngeal cavity from contributing much in that capacity (Lieberman et al., 1969, Lieberman, 1984, Fitch, 2000a, Fitch and Hauser, 2003). Thus, nonhuman mammals have physical constraints to any rapid sequential modification of the cross-sectional areas of the SVT. In contrast, adult humans have an equally long SVTH and SVTV. Their epiglottis is separated from the velum, and this produces a long oropharyngeal region facing the dorsal surface of the tongue, rostral to the laryngopharyngeal region that faces the epiglottis (Lieberman, 1984, Crelin, 1987, Zemlin, 1988, Titze, 1994). The vertical dimension of the tongue is almost equal to the horizontal dimension to fit this configuration, and the internal musculature of the tongue makes the surface highly mobile (Takemoto, 2001). In anatomical terms, these features allow the shapes of the SVTH and SVTV to be sequentially and rapidly modified by tongue movements, semi-independently of each other (Lieberman et al., 1969, Lieberman, 1984, Fitch, 2000a, Fitch and Hauser, 2003). Thus, humans are capable of extensive modification of the resonant properties of the SVT, which in turn modify the laryngeal sounds, forming the complex sequential phonemes of speech in a single, short exhalation.
In newborn humans, the larynx is positioned close to the palate so there is little vertical pharyngeal space (Negus, 1949, Lieberman, 1984, Crelin, 1987, Lieberman et al., 2001). However, the major descent of the larynx causes the epiglottis to descend relative to the velum (Negus, 1949, Roche and Barkla, 1965, Sasaki et al., 1977, Crelin, 1987, Westhorpe, 1987, Fitch and Giedd, 1999, Vorperian et al., 1999, Vorperian et al., 2005). This establishes a long oropharyngeal space, rostral to the laryngopharyngeal region in the SVTV. Thus, the SVTV lengthens rapidly compared with the SVTH, and can function as a resonance tube of equivalent volume (Lieberman, 1984, Crelin, 1987, Titze, 1994, Fitch, 2000a).
The laryngeal skeleton is suspended from the hyoid apparatus, and the hyoid is in turn suspended from the mandible and cranial base by muscles and ligaments (Zemlin, 1988). Anatomically, two processes accomplish the descent of the larynx: the descent of the laryngeal skeleton relative to the hyoid, and the descent of the hyoid relative to the palate. This process has been evaluated with detailed measurements on humans from X-ray photographs (Lieberman and McCarthy, 1999, Lieberman et al., 2001) and magnetic resonance imaging (MRI; Fitch and Giedd, 1999, Vorperian et al., 1999, Vorperian et al., 2005). We have studied the development of three living chimpanzees using MRI. Our previous study compared the growth of the SVT in chimpanzees and humans during the first two years of life, and showed that—as in humans—chimpanzees show rapid laryngeal descent, with changes in the relative proportion of the SVTH and SVTV (Nishimura et al., 2003). Another MRI study (Nishimura, 2005), using a cross-sectional ontogenetic series of embalmed specimens, confirmed this developmental change during early infancy. However, that study also showed that the larynx is lowered only slightly and the horizontal oral cavity grows largely during the juvenile period, causing the proportion of the SVT in chimpanzees to differ from that in humans. Unfortunately, embalming artifacts precluded the study of developmental changes in the position of the hyoid and epiglottis relative to the palate. Therefore, the descent of the chimpanzee larynx is considered to depend primarily on the descent of the laryngeal skeleton relative to the hyoid, but not on the descent of the hyoid per se (Nishimura et al., 2003, Nishimura, 2005). Thus, the human 1:1 proportion of the SVTH to SVTV is still believed to depend on the greater proportional descent of the hyoid during the evolution of the human lineage (Negus, 1949, Lieberman, 1984, Crelin, 1987, Flügel and Rohen, 1991, Houghton, 1993, Laitman and Reidenberg, 1993, Nishimura, 2003, Nishimura, 2005, Nishimura et al., 2003). In fact, the term “descent” of the larynx or hyoid often implies the proportional changes of SVT toward such a configuration (here we use the terms “descent” and “descend” without any such implication). Here, we used MRI to evaluate the developmental changes in SVT anatomy in three living chimpanzees aged between two-and-a-half and five years, and we use the results to discuss the evolution of the descent of the larynx.
Section snippets
MRI procedures
We have studied the development of three living chimpanzees, named Ayumu (male), Cleo (female), and Pal (female), using MRI. They were born in 2000 and were reared by the biological mothers in the Primate Research Institute (PRI), Kyoto University, Japan (Matsuzawa, 2003). The care and use of the subjects conformed to the guidelines of the Primate Research Institute, 1986, Primate Research Institute, 2002. The chimpanzees were scanned at scheduled intervals from four months to five years of age
Results
The scan for Ayumu at 52 months of age showed that, at the time of scanning, the tongue was contracted anterosuperiorly, probably causing additional elevation of the hyoid and larynx (Fig. 3; Appendix 2). Although this indicates the dynamic anatomy of the chimpanzee vocal tract (discussed below), the scan was excluded from the analyses of the developmental changes in resting anatomy of the SVT.
In chimpanzees, the SVTV increases more than the SVTH during early infancy (Nishimura et al., 2003),
Discussion
This study provides no evidence for the idea that the rapid descent of the larynx or hyoid arose uniquely in the human lineage to allow the configuration of the equally long SVTH and SVTV to develop and thus permit the acquisition of speech in this lineage (Negus, 1949, Lieberman, 1984, Crelin, 1987, Houghton, 1993, Laitman and Reidenberg, 1993, Nishimura, 2003, Nishimura, 2005, Nishimura et al., 2003). Some gross anatomical studies using a cross-sectional ontogenetic series of embalmed
Conclusions
The major descent of the larynx and the reduced growth of the face essentially constitute the “ontogeny” of the morphological foundations of speech in humans (Negus, 1949, Lieberman, 1984, Crelin, 1987, Zemlin, 1988, Flügel and Rohen, 1991, Laitman and Reidenberg, 1993, Fitch and Giedd, 1999, Lieberman et al., 2001). However, this study does not support the “evolutionary” hypothesis that this descent occurred in the human lineage, and thereby produced the SVT configuration with an equally long
Acknowledgments
We are grateful to A. Kato, K. Kumazaki, N. Maeda, S. Goto, K. Matsubayashi, M. Tomonaga, M. Tanaka, Y. Hamada, and the staff of PRI for daily veterinary care for the three chimpanzees and/or support for the MRI examinations. We thank D.E. Lieberman and his colleagues for kindly permitting us to use the numerical data from D.E. Lieberman et al. (2001). Portions of this work were performed at PRI under 2004 and 2005 PRI Cooperative Research Programs (Grant 4-1 and 3-1 to T. N.). This work was
References (67)
The evolution of speech: a comparative review
Trends Cogn. Sci.
(2000)- et al.
The craniofacial proportions and laryngeal position in monkeys and man of different ages. (A morphometric study based on CT-scans and radiographs)
Mech. Aging Dev.
(1991) - et al.
The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions
J. Hum. Evol.
(1999) - et al.
Ontogeny of postnatal hyoid and larynx descent in humans
Arch. Oral Biol.
(2001) - et al.
Vocal production mechanisms in a non-human primate: morphological data and a model
J. Hum. Evol.
(2005) - et al.
Magnetic resonance imaging procedures to study the concurrent anatomic development of vocal tract structures: preliminary results
Int. J. Pediatr. Otorhinolaryngol.
(1999) - et al.
Common patterns of facial ontogeny in the hominid lineage
Anat. Rec.
(2002) Terrestriality, bipedalism and the origin of language
The foundations of human language
- et al.
An Introduction to Human Evolutionary Anatomy
(1998)
Kehlkopf und Kehlsack des Schimpansen (Pan troglodytes)
Gegenbaurs. Morphol. Jahrb.
Mixed longitudinal study of dental emergency in the chimpanzee, Pan troglodytes (Primates, Pongidae)
Am. J. Phys. Anthropol.
The Human Vocal Tract
Textbook of Veternary Anatomy
Facial Growth
Acoustic Theory of Speech Production
The phonetic potential of nonhuman vocal tracts: comparative cineradiographic observations of vocalizing animals
Phonetica
Morphology and development of the human vocal tract: a study using magnetic resonance imaging
J. Acoust. Soc. Am.
Unpacking “Honesty”: vertebrate vocal production and the evolution of acoustic signals
The descended larynx is not uniquely human
Proc. R. Soc. Lond. B Biol. Sci.
Primate Adaptation and Evolution
The Saccus laryngis in primates
J. Anthropol. Soc. Nippon
The functions of laryngeal air sac in primates: a new hypothesis
Folia Primatol.
Food transport and bolus formation during complete feeding sequences on foods of different initial consistency
Dysphagia
Neandertal supralaryngeal vocal tract
Am. J. Phys. Anthropol.
Ranges of normalcy in the eruption of permanent teeth
J. Dent. Child.
Eruption of deciduous teeth in Japanese macaques (Macaca fuscata)
J. Anthropol. Soc. Nippon
Studies on the structure of the organ of voice and vocalization in the chimpanzees, part 1
Folia Morphol. (Warzs)
The anatomical basis of phonation in the chimpanzee
J. Morphol.
The Human Career
Probit and survival analysis of tooth emergency ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes)
Am. J. Phys. Anthropol.
The basicranium of Plio-Pleistocene hominids as an indicator of their upper respiratory systems
Am. J. Phys. Anthropol.
Specialization of the human upper respiratory and upper digestive system as seen through comparative and developmental anatomy
Dysphasia
Cited by (58)
Comparative Histoanatomy of the Epiglottis and Preepiglottic Space of the Lemur Larynx
2022, Journal of VoiceCitation Excerpt :Some species of non-human primates, such as chimpanzees, have a descended larynx.8 The larynx descends against the head and jaw through a varied combination of the descent of the hyoid against the palate and the descent of the larynx against the hyoid.9-13 On the other hand, the larynx of some non-human primates, such as lemurs, have a limited vocal tract and pharyngeal space and does not descend.14
The effects of larynx height on vowel production are mitigated by the active control of articulators
2019, Journal of PhoneticsThe baboon: A model for the study of language evolution
2019, Journal of Human EvolutionCitation Excerpt :For instance, it is now well known that human babies, who also have a high larynx, produce the same vocalic range as adults (De Boysson-Bardies et al., 1989). In addition, low larynxes have been discovered in animal species (chimpanzee, ruminant) with no documented ability to produce systems of vowel-like sounds (e.g., Nishimura et al., 2006). In one of our recent studies (Boë et al., 2017b), we investigated whether nonhuman primates can produce a much richer set of distinct vowel-like vocalizations than predicted by the descent of larynx hypothesis.
Language and human evolution
2017, Journal of NeurolinguisticsArdipithecus ramidus and the evolution of language and singing: An early origin for hominin vocal capability
2017, HOMO- Journal of Comparative Human BiologyCitation Excerpt :Consequently, humans have a smaller horizontal dimension than chimpanzees but also a larger vertical dimension (Nishimura et al., 2006). In humans facial flattening (Nishimura et al., 2006) and erect posture (Negus, 1949) seem to be two major anatomical factors contributing to the vocal tract configuration. Further, the anatomy of the human vertebral column associated with erect posture also indirectly facilitates speech production.