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The Shape of Sound: a Geometric Morphometrics Approach to Laryngeal Functional Morphology

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Abstract

Diversification of animal vocalizations plays a key role in behavioral evolution and speciation. Vocal organ morphology represents an important source of acoustic variation, yet its small size, complex shape, and absence of homologous landmarks pose major challenges to comparative analyses. Here, we use a geometric morphometric approach based on geometrically homologous landmarks to quantify shape variation of laryngeal cartilages of four rodent genera representing three families. Reconstructed cartilages of the larynx from contrast-enhanced micro-CT images were quantified by variable numbers of three-dimensional landmarks placed on structural margins and major surfaces. Landmark sets were superimposed using generalized Procrustes analysis prior to statistical analysis. Correlations among pairwise Procrustes distances were used to identify the minimum number of landmarks necessary to fully characterize shape variation. We found that the five species occupy distinct positions in morphospace, with variation explained in part by phylogeny, body size, and differences in vocal production mechanisms. Our findings provide a foundation for quantifying the contribution of vocal organ morphology to acoustic diversification.

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References

  • Adams DC, Collyer ML, Kaliontzopoulou A, Sherratt E (2017) Geomorph: software for geometric morphometric analyses. R package version 3.0.5. (https://cran.r-project.org/package=geomorph.). Accessed July 2017

  • Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix 24:7–14

  • Ajmani ML (1990) A metrical study of the laryngeal skeleton in adult Nigerians. J Anat 171:187–191

  • Baab KL, McNulty KP, Rohlf FJ (2012) The shape of human evolution: A geometric morphometrics perspective. Evolutionary Anthropology 21:151-165

  • Bartholomew GR, Caswell HH (1959) Locomotion in kangaroo rats and its adaptive significance. J Mammal 32:155–169

  • Bailey V, Sperry C (1929) Life history and habits of grasshopper mice, genus Onychomys. Technical Bulletin Dept Agriculture 145:1-19.

  • Beasley De AE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indicat 30:218–226

  • Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge

  • Bookstein FL (1997) Morphometric Tools for Landmark Data. Morphometry and Biology. Cambridge University Press, Cambridge

  • Bookstein FL, Streissguth AP, Sampson PD, Connor PD, Barr HM (2002) Corpus callosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. Neuroimage 15:233–251

  • Botton-Divet L, Houssaye A, Herrel A, Fabre AC, Cornette R (2015) Tools for quantitative form description; an evaluation of different software packages for semi-landmark analysis. PeerJ 3:e1417

  • Bradbury JW, Vehrencamp SL (2011) Principles of Animal Communication (2nd edition). Sinauer Associates, Sunderland

  • Bramble DM, Carrier DR (1983) Running and breathing in mammals. Science 219:251–256

  • Brown CH, Riede T (2017) An introduction to laryngeal biomechanics. In: Brown CH, Riede T (eds) Comparative Bioacoustics: An Overview. Bentham Science Publishers, Oak Park, pp 120–164

  • Brudzynski SM (2005) Principles of rat communication: quantitative parameters of ultrasonic calls in rats. Behav Genet 35:85–92

  • Cap H, Deleporte P, Joachim J, Reby D (2008) Male vocal behavior and phylogeny in deer. Cladistics 24:917–931

  • Clarke JA, Chatterjee S, Li Z, Riede T, Agnolin F, Goller F, Isasi MP, Martinioni DR, Mussel FJ Novas F (2016) Fossil evidence of the avian vocal organ from the Mesozoic. Nature 538:502–505

  • Denny SP (1976) Comparative anatomy of the larynx. In: Hinchcliffe R, Harrison DNF (eds) Scientific Basis of Otolaryngology. Heinemann, London, pp 536–545

  • Eckel HD, Sittel C (1995) Morphometry of the larynx in horizontal sections. Am J Otolaryngol 16:40–48

  • Eckel HE, Sittel C, Zorowka P, Jerke A (1994) Dimensions of the laryngeal framework in adults. Surg Radiol Anat 16:31–36

  • Frable MA (1961) Computation of motion at the cricoarytenoid joint. Arch Oto-laryngol 73:73–78

  • Gower JC (1975) Generalized procrustes analysis. Psychometrika 40:33–51

  • Gunz P, Mitteroecker P (2013) Semilandmarks: a method for quantifying curves and surfaces. Ital J Mammal 24:103–109

  • Harrison DFN (1995) The Anatomy and Physiology of the Mammalian Larynx. Cambridge University Press, Cambridge

  • Hatt RT (1932) The vertebral column of ricochetal rodents. Bull Am Mus Nat Hist 63:599–745

  • Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3(12):e386

  • Hunter E, Titze IR (2005) Individual subject laryngeal dimensions of multiple mammalian species for biomechanical models. Ann Otol Rhinol Laryngol 114:809–818

  • Hunter EJ, Titze IR, Alipour F (2004) A three-dimensional model of vocal fold abduction/adduction. J Acoust Soc Am 115:1747–1759

  • Jain M, Dhall U (2008) Morphometry of the thyroid and cricoid cartilages in adults. J Anat Soc India 57:119–123

  • Jourdan D, Ardid D, Chapuy E, Eschalier A, LeBars D (1995) Audible and ultrasonic vocalization elicited by single electrical nociceptive stimuli to the tail in the rat. Pain 63:237–249

  • Jotz GP, Stefani MA, Pereira da Costa Fihlo O, Malysz T, Soster PR, Leao HZ (2014) The morphometric study of the larynx. J Voice 28:668–672

  • Jürgens U (2009) The neural control of vocalization in mammals: a review. J Voice 23:1–10

  • Klingenberg CP (2008) Novelty and “homology-free” morphometrics: what’s in a name? Evol Biol 35:186–190

  • Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934

  • Laitman JT, Noden DM, van de Water TR (2014) Formation of the larynx: from Hox genes to critical periods. In: Rubin JS, Sataloff RT, Korovin GS (eds) Diagnosis and Treatment of Voice Disorders. 4th edition. Plural Publishing, San Diego

  • Langley WM (2008) Grasshopper Mouse: Evolution of a Carnivorous Lifestyle. Lulu Press, Morrisville, NC

  • Loth A, Corny J, Santini L, Dahan L, Dessi P, Adalian P, Fakhry N (2015) Analysis of hyoid-larynx complex using 3D geometric morphometric. Dysphagia 30:357–354

  • Luo B, Huang X, Li Y, Lu G, Zhao J, Zhang K, Zhao H, Liu Y, Feng J (2017) Social call divergence in bats: a comparative analysis. Behav Ecol 28:533–540

  • Macdonald D, Norris S (2001) The New Encyclopedia of Mammals. Oxford University Press, Oxford

  • McLeod G (2015) Use of landmark and outline morphometrics to investigate thecal form variation in crushed gogiid echinoderms. Palaeoworld 24:408–429

  • Metscher BD (2009) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9:1

  • Miller JR, Engstrom MD (2012) Vocal stereotypy in the rodent genera Peromyscus and Onychomys (Neotominae): taxonomic signature and call design. Bioacoustics 21:193–213

  • Moisik SR, Gick B (2017) The quantal larynx: the stable regions of laryngeal biomechanics and implications for speech production. J Speech Language Hear Res 60:540–560

  • Negus VE (1949). The Comparative Anatomy and Physiology of the Larynx. Grune and Stratton Inc, New York

  • Palaparthi A, Riede T, Titze IR (2014) Combining multi-objective optimization and cluster analysis to study vocal fold functional morphology. IEEE Trans Biomed Eng 61:2199–2208

  • Pasch B, George AS, Hamlin HJ, Guillette LJ, Phelps SM (2011) Androgens modulate song effort and aggression in Neotropical singing mice. Horm Behav 59:90–97

  • Pasch B, Tokuda IT, Riede T (2017) Grasshopper mice employ distinct vocal production mechanisms in different social contexts. Proc Roy Soc Lond B 284:20171158

  • Plotsky K, Rendall D, Chase K, Riede T (2016) Cranio-facial remodeling in domestic dogs is associated with changes in larynx position. J Anatomy 228:975-983

  • Pergams ORW, Lawler JJ (2009) Recent and Widespread Rapid Morphological Change in Rodents. PLoS ONE 4:e6452.

  • R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Randall JA (1994) Discrimination of footdrumming signatures by kangaroo rats, Dipodomys spectabilis. Anim Behav 47:45–54

  • Riede T (2013) Call type specific motor patterns in rat ultrasound vocalization. J Exp Zool A 319:213–224

  • Riede T (2018) Peripheral vocal motor dynamics and combinatory call complexity of ultrasonic vocal production in rats. In: Brudzynski S (editor) Handbook of Behavioral Neuroscience. Elsevier 25:45-60

  • Riede T, Borgard HL, Pasch B (2017) Laryngeal airway reconstruction indicates rodent ultrasonic vocalizations are produced by an edge tone mechanism. R Soc Open Science 4:170976

  • Rieger NS, Marler CA (2018) The function of ultrasonic vocalizations during territorial defence by pair-bonded male and female California mice. Anim Behav 135:97–108

  • Roberts LH (1975) The functional anatomy of the rodent larynx in relation to audible and ultrasonic cry production. Zool J Linn Soc 56:255–264

  • Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Classif 16:197–223

  • Rohlf FJ, Slice D (1990) Extension of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

  • Roth G, Levine MD (1993) Extracting geometric primitives. CVGIP: Image Understanding 58:1–22

  • Samuels JX (2009) Cranial morphology and dietary habits of rodents. Zool J Linnean Soc 156:864–888

  • Satoh K, Iwaku F (2006) Jaw muscle functional anatomy in northern grasshopper mouse, Onychomys leucogaster, a carnivorous murid. J Morphol 267:987–999

  • Schild JA (1984) Relationship of laryngeal dimensions to body size and gestational age in premature neonates and small infants. Laryngoscope 94:1284–1292

  • Schneider R (1964) Der Larynx der Säugetiere. Handbuch der Zoologie 5:1–128

  • Sellars IE, Keen EN. (1978) The anatomy and movements of the cricoarytenoid joint. Laryngoscope 88:667–674

  • Shelley EL, Blumstein DT (2004) The evolution of vocal alarm communication in rodents. Behavioral Ecology 16:169–177

  • Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, Schmeidler J, Gasperi R, Gama Sosa MA, Rabidou D, Santucci AC, Perl D, Morrisey E, Buxbaum JD (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci USA 10:9643–9648

  • Sprinzl GM, Eckel HE, Sittel C, Pototschnig C, Koebke J (1999) Morphometric measurements of the cartilaginous larynx: an anatomic correlate of laryngeal surgery. Head Neck 21:743–750

  • Storck C, Juergens P, Fischer C, Wolfensberger M, Honegger F, Sorantin E, Friedrich G, Gugatschka M (2011) Biomechanics of the cricoarytenoid joint: three-dimensional imaging and vector analysis. J Voice 25:406–410

  • Storck C, Unteregger F (2018) Cricothyroid joint type as predictor for vocal fold elongation in professional singers. Laryngoscope 128:1176–1181

  • Tayama N, Chan RW, Kaga K, Titze IR (2001) Geomtric characterization of the laryngeal cartilage framework for the purpose of biomechanical modeling. Ann Otol Rhinol Laryngol 110:1154–1161

  • Titze IR (2000) Principals of Voice Production. National Center for Voice and Speech, Salt Lake City

  • Titze IR, Riede T, Mau T (2016) Predicting fundamental frequency ranges in vocalizations across species. PLoS Comp Biol 12:e1004907

  • Tabler JM, Rigney MM, Berman GJ, Gopalakrishnan S, Heude E, Al-Lami HA, Yannakoudakis BZ, Fitch RD, Carter CM, Vokes SA, Liu KJ, Tajbakhsh S, Egnor SER, Wallingford JB (2017) Cilia-mediated hedgehog signaling controls form and function in the mammalian larynx. eLife 6:e19153.

  • Unteregger F, Honegger F, Potthast S, Zwicky S, Schiwowa J, Storck C (2017) 3D Analysis of the Movements of the Laryngeal Cartilages During Singing. Laryngoscope 127:1639–1643

  • Vilkman E, Sonninen A, Hurme P, Korkko P (1996) External laryngeal frame function in voice production revisited: a review. J Voice 10:78–92.

  • Von Leden H, Moore P. (1961) The mechanics of the cricoarytenoid joint. Arch Otolaryngol 73:541–550.

  • Wärmländer SKTS, Garvin H, Guyomarc'h P, Petaros A, Sholts SB (2019) Landmark Typology in Applied Morphometrics Studies: What's the Point?  The Anatomical Record. https://doi.org/10.1002/ar.24005

  • Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28:156–166.

  • Williams SH, Pfeiffer E, Ford S (2009) Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: does jaw-muscle anatomy predict performance? J Morphol 270:1338–1347

  • Zelditch ML, Lundrigan BL, Garland T Jr (2004) Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evol Dev 6:194–2063

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The study was supported by the National Science Foundation (award number 1754332).

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Correspondence to Tobias Riede.

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Borgard, H.L., Baab, K., Pasch, B. et al. The Shape of Sound: a Geometric Morphometrics Approach to Laryngeal Functional Morphology. J Mammal Evol 27, 577–590 (2020). https://doi.org/10.1007/s10914-019-09466-9

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