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Complexity from simplification

Human speech and language are highly complex, consisting of a large number of sounds. The human phonal apparatus, the larynx, has acquired the capability to create a wider array of sounds, even though previous work has revealed many similarities between our larynx and those in other primates. Looking across a large number of primates, Nishimura et al. used a combination of anatomical, phonal, and modeling approaches to characterize sound production in the larynx (see the Perspective by Gouzoules). They found that instead of the human larynx having increased complexity, it has actually simplified relative to other primates, allowing for clearer sound production with less aural chaos. —SNV

Abstract

Human speech production obeys the same acoustic principles as vocal production in other animals but has distinctive features: A stable vocal source is filtered by rapidly changing formant frequencies. To understand speech evolution, we examined a wide range of primates, combining observations of phonation with mathematical modeling. We found that source stability relies upon simplifications in laryngeal anatomy, specifically the loss of air sacs and vocal membranes. We conclude that the evolutionary loss of vocal membranes allows human speech to mostly avoid the spontaneous nonlinear phenomena and acoustic chaos common in other primate vocalizations. This loss allows our larynx to produce stable, harmonic-rich phonation, ideally highlighting formant changes that convey most phonetic information. Paradoxically, the increased complexity of human spoken language thus followed simplification of our laryngeal anatomy.

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References and Notes

1
A. M. Taylor, D. Reby, The contribution of source-filter theory to mammal vocal communication research. J. Zool.280, 221–236 (2010).
2
C. T. Herbst, A. S. Stoeger, R. Frey, J. Lohscheller, I. R. Titze, M. Gumpenberger, W. T. Fitch, How low can you go? Physical production mechanism of elephant infrasonic vocalizations. Science337, 595–599 (2012).
3
H. Koda, I. T. Tokuda, M. Wakita, T. Ito, T. Nishimura, The source-filter theory of whistle-like calls in marmosets: Acoustic analysis and simulation of helium-modulated voices. J. Acoust. Soc. Am.137, 3068–3076 (2015).
4
C. P. Elemans, J. H. Rasmussen, C. T. Herbst, D. N. Düring, S. A. Zollinger, H. Brumm, K. Srivastava, N. Svane, M. Ding, O. N. Larsen, S. J. Sober, J. G. Švec, Universal mechanisms of sound production and control in birds and mammals. Nat. Commun.6, 8978 (2015).
5
W. T. Fitch, The evolution of speech: A comparative review. Trends Cogn. Sci.4, 258–267 (2000).
6
W. T. Fitch, J. Neubauer, H. Herzel, Calls out of chaos: The adaptive significance of nonlinear phenomena in mammalian vocal production. Anim. Behav.63, 407–418 (2002).
7
U. Jürgens, Neural pathways underlying vocal control. Neurosci. Biobehav. Rev.26, 235–258 (2002).
8
I. R. Titze, Principles of Voice Production (Prentice Hall, 1994).
9
K. N. Stevens, Acoustic Phonetics (MIT Press, 1998).
10
P. H. Lieberman, D. H. Klatt, W. H. Wilson, Vocal tract limitations on the vowel repertoires of rhesus monkey and other nonhuman primates. Science164, 1185–1187 (1969).
11
P. Lieberman, The evolution of human speech: Its anatomical and neural bases. Curr. Anthropol.48, 39–66 (2007).
12
T. Nishimura, A. Mikami, J. Suzuki, T. Matsuzawa, Descent of the larynx in chimpanzee infants. Proc. Natl. Acad. Sci. U.S.A.100, 6930–6933 (2003).
13
S. Hayama, The Saccus laryngis in primates. J. Anthrol. Soc. Jpn.78, 274–298 (1970).
14
Z. Alemseged, F. Spoor, W. H. Kimbel, R. Bobe, D. Geraads, D. Reed, J. G. Wynn, A juvenile early hominin skeleton from Dikika, Ethiopia. Nature443, 296–301 (2006).
15
S. Hayama, “From what period did the formation of human glottal tones originate?” in Primatology Today, A. Ehara, T. Kimura, O. Takenaka, M. Iwamoto, Eds. (Elsevier, 1991), pp. 491–492.
16
P. Mergell, W. T. Fitch, H. Herzel, Modeling the role of nonhuman vocal membranes in phonation. J. Acoust. Soc. Am.105, 2020–2028 (1999).
17
Y. S. Zhang, D. Y. Takahashi, D. A. Liao, A. A. Ghazanfar, C. P. H. Elemans, Vocal state change through laryngeal development. Nat. Commun.10, 4592 (2019).
18
D. Rendall, M. J. Owren, P. S. Rodman, The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. J. Acoust. Soc. Am.103, 602–614 (1998).
19
P. Marler, R. Tenaza, “Signaling behavior of apes with special reference to vocalization,” in How Animals Communicate, T. A. Sebeok, Ed. (Indiana Univ. Press, Bloomington, 1977), pp. 965–1033.
20
K. Ishizaka, J. L. Flanagan, Synthesis of voiced sounds from a 2-mass model of the vocal cords. Bell Syst. Tech. J.51, 1233–1268 (1972).
21
J. Neubauer, “Nonlinear dynamics of the voice: Bifurcations and mode analysis of complex spatio-temporal signals,” thesis, Humboldt University of Berlin (2004).
22
I. T. Tokuda, Non-linear dynamics in mammalian voice production. Anthropol. Sci.126, 35–41 (2018).
23
P. Berg, Y. Pomeau, C. Vidal, Order within Chaos: Towards a Deterministic Approach to Turbulence (Wiley, 1986).
24
L. Glass, M. C. Mackey, From Clocks to Chaos: The Rhythms of Life (Princeton Univ. Press, 1988).
25
M. J. Owren, D. Rendall, Salience of caller identity in rhesus monkey (Macaca mulatta) coos and screams: Perceptual experiments with human (Homo sapiens) listeners. J. Comp. Psychol.117, 380–390 (2003).
26
W. T. Fitch, J. B. Fritz, Rhesus macaques spontaneously perceive formants in conspecific vocalizations. J. Acoust. Soc. Am.120, 2132–2141 (2006).
27
W. Mende, H. Herzel, K. Wermke, Bifurcations and chaos in newborn infant cries. Phys. Lett. A145, 418–424 (1990).
28
H. Herzel, D. Berry, I. R. Titze, M. Saleh, Analysis of vocal disorders with methods from nonlinear dynamics. J. Speech Hear. Res.37, 1008–1019 (1994).
29
P. M. Gignac, N. J. Kley, J. A. Clarke, M. W. Colbert, A. C. Morhardt, D. Cerio, I. N. Cost, P. G. Cox, J. D. Daza, C. M. Early, M. S. Echols, R. M. Henkelman, A. N. Herdina, C. M. Holliday, Z. Li, K. Mahlow, S. Merchant, J. Müller, C. P. Orsbon, D. J. Paluh, M. L. Thies, H. P. Tsai, L. M. Witmer, Diffusible iodine-based contrast-enhanced computed tomography (diceCT): An emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J. Anat.228, 889–909 (2016).
30
W. P. Maddison, D. R. Maddison, Mesquite: a modular system for evolutionary analysis. Version 3.61 (2018). http://www.mesquiteproject.org
31
J. Li, K. Han, J. Xing, H.-S. Kim, J. Rogers, O. A. Ryder, T. Disotell, B. Yue, M. A. Batzer, Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. Gene 448, 242–249 (2009).
32
P. Perelman, W. E. Johnson, C. Roos, H. N. Seuánez, J. E. Horvath, M. A. M. Moreira, B. Kessing, J. Pontius, M. Roelke, Y. Rumpler, M. P. C. Schneider, A. Silva, S. J. O’Brien, J. Pecon-Slattery, A molecular phylogeny of living primates. PLOS Genet.7, e1001342 (2011).
33
Z. Takacs, J. C. Morales, T. Geissmann, D. J. Melnick, A complete species-level phylogeny of the Hylobatidae based on mitochondrial ND3-ND4 gene sequences. Mol. Phylogenet. Evol. 36, 456–467 (2005).
34
S. Kurita, K. Nagata, M. Hirano, “A comparative study of the layer structure of the vocal fold,” in Vocal Fold Physiology: Contemporary Research and Clinical Issues, D. M. Bless, J. H. Abbs, Eds. (College-Hill Press, San Diego, 1983), pp. 3–21.
35
M. Hirano, Morphological structure of the vocal cord as a vibrator and its variations. Folia Phoniatr. 26, 89–94 (1974).

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Science
Volume 377 | Issue 6607
12 August 2022

Submission history

Received: 30 August 2021
Accepted: 30 June 2022
Published in print: 12 August 2022

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Acknowledgments

We are grateful to the late Sugio Hayama for conceiving and conducting in vivo chimpanzee experiments and for establishing the collection of excised larynges at the Japan Monkey Centre (JMC). We thank the JMC, Nagoya Higashiyama Zoo, Fukuoka City Zoological Garden, Kagoshima City Hirakawa Zoological Park, Yokohama Zoological Gardens, and the Wildlife Research Center, the Laboratory of Physical Anthropology, and the Primate Research Institute (PRI) of Kyoto University for providing samples. We thank T. Udono, Y. Shintaku, K. Matsui, H. Imai, S. Tsubouchi, and A. Kataoka for preparing or scanning the specimens; Y. Nomura and Z. Chen for examining laryngeal anatomy; K. Migimatsu, T. Matsumoto, M. Kanaya, and R. Miyazaki for conducting ex vivo experiments; C. R. Larson for providing suggestions for in vivo experiments of macaques; and T. Miyabe-Nishiwaki, Y. Sawada, B. Bach Andersen, and present and past staff of the PRI and the German Primate Center for help conducting in-vivo experiments and/or daily care of subjects. We appreciate the photograph courtesy of K. Sato at the Kurume University. This research was in part supported by the Kyoto University-University of Vienna Strategic Partnership Program.
Funding: Japan Society for the Promotion of Science grants 16H04848 and 19H01002 (T.N.), 17H06313 and 20K11875 (I.T.T.), and 18H03503 (H.K.) Research Units for Exploring Future Horizons through the Kyoto University Research Coordination Alliance (T.N., C.T.H.) Rhinology and Laryngology Research Fund UK (J.C.D.) Ministry of Education, Culture, Sports, Science and Technology Grant-in-aid for Scientific Research on Innovative Areas no. 4903 (Evolinguistics) grant 17H06380 (H.K.) Ministry of Education, Culture, Sports, Science and Technology Grant-in-aid for Scientific Research on Innovative Areas no. 4903 (Evolinguistics) (W.T.F.) Austrian Science Fund DK Grant “Cognition & Communication 2” grant W1262-B29 (W.T.F.).
Author contributions: Conceptualization: T.N., W.T.F. Methodology: T.N., C.T.H., I.T.T., S.M., J.C.D., U.J., W.T.F., O.N.L. Formal analysis: T.N., I.T.T., W.T.F. Investigation: T.N., W.T.F., I.T.T., S.M., J.C.D., C.T.H., K.I., A.K., Y.K., H.K., J.P.P.S., H.I., T.M., O.N.L., U.J., H.H., S.K. Resources: T.N., A.K., U.J., S.K., O.N.L. Writing - original draft: T.N., I.T.T., S.M., J.C.D., C.T.H., W.T.F. Writing - review and editing: T.N., I.T.T., W.T.F. Project administration: T.N. Funding acquisition: T.N., I.T.T., J.C.D., H.K., W.T.F.
Competing interests: The authors declare that they have no competing interests.
Data and materials availability: Laryngeal specimens from the subjects named Baran, Keiko, Wilie, and Yuri were available from the zoos under a material transfer agreement with the Kyoto University. Some specimens were provided through the Collaborative Research program of the JMC (no. 2018017) and the Great Ape Information Network under the National BioResource Project (NBRP) of Japan. All data are available in the main text or the supplementary materials.
License information: Copyright © 2022 the authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original US government works. https://www.science.org/about/science-licenses-journal-article-reuse

Authors

Affiliations

Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Roles: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, and Writing - review & editing.
Department of Mechanical Engineering, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan.
Roles: Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Software, Validation, Visualization, Writing - original draft, and Writing - review & editing.
Shigehiro Miyachi
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Roles: Investigation, Methodology, Validation, and Writing - original draft.
Behavioural Ecology Research Group, School of Life Science, Anglia Ruskin University, Cambridge CB1 1PT, UK.
Department of Archaeology, University of Cambridge, Cambridge CB2 3DZ, UK.
Department of Behavioral and Cognitive Biology, University of Vienna, 1030 Vienna, Austria.
Roles: Funding acquisition, Investigation, Methodology, Writing - original draft, and Writing - review & editing.
Christian T. Herbst
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Department of Behavioral and Cognitive Biology, University of Vienna, 1030 Vienna, Austria.
Roles: Conceptualization, Formal analysis, Investigation, Methodology, Resources, Software, Validation, Writing - original draft, and Writing - review & editing.
Kazuyoshi Ishimura
Department of Mechanical Engineering, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan.
Role: Investigation.
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Roles: Investigation and Resources.
Yuki Kinoshita
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Role: Investigation.
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Roles: Data curation, Funding acquisition, Investigation, and Resources.
Present address: Department of Life Science, Graduate School of Arts and Sciences, The University of Tokyo, Meguro, Tokyo 153-8902, Japan.
Department of Archaeology, University of Cambridge, Cambridge CB2 3DZ, UK.
Role: Investigation.
Department of Systems Science, Graduate School of Informatics, Kyoto University, Sakyo, Kyoto 606-8501, Japan.
Role: Investigation.
Department of Systems Science, Graduate School of Informatics, Kyoto University, Sakyo, Kyoto 606-8501, Japan.
Role: Investigation.
Department of Biology, University of Southern Denmark, DK-5230 Odense M, Denmark.
Roles: Data curation, Investigation, Methodology, Resources, and Validation.
Uwe Jürgens
Section of Neurobiology, German Primate Center, D-37077 Göttingen, Germany
Roles: Investigation, Methodology, and Resources.
Hideki Hirabayashi
Dokkyo Medical University, Mibu, Tochigi 321-0293, Japan.
Role: Investigation.
Shozo Kojima
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Roles: Investigation and Resources.
Department of Behavioral and Cognitive Biology, University of Vienna, 1030 Vienna, Austria.
Cognitive Science Hub, University of Vienna, Vienna, Austria.
Roles: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Validation, Writing - original draft, and Writing - review & editing.

Funding Information

Ministry of Education, Culture, Sports, Science and Technology Grant-in-aid for Scientific Research on Innovative Areas #4903 (Evolinguistics)
Austrian Science Fund DK Cognition and Communication WTF: W1262-B29
Ministry of Education, Culture, Sports, Science and Technology Grant-in-aid for Scientific Research on Innovative Areas #4903 (Evolinguistics): 17H06380

Notes

*
Corresponding author. Email: [email protected] (T.N.); [email protected] (W.T.F.)

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  1. When less is more in the evolution of language, Science, 377, 6607, (706-707), (2022)./doi/10.1126/science.add6331
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