Sexual Dimorphism of the Zebra Finch Syrinx Indicates Adaptation for High Fundamental Frequencies in Males

Abstract

BackgroundIn many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.Methodology/Principal FindingsHere we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.Conclusions/SignificanceThe syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.

A Mechanism for Frequency Modulation in Songbirds Shared with Humans

“…Many descriptions of voiced sound production are based on the seminal work by Titze (1988Titze ( , 1994, who described a model to account for the vocal folds motion in humans. Given the anatomical and functional similarities between the vocal apparatus of humans and birds (Riede and Goller, 2010), this description helps to capture essential features of birdsong production. Direct endoscopic observation showed that phonation was initiated in the songbird syrinx when two soft tissue masses, the medial and lateral labia, were pushed into the bronchial lumen (Goller and Larsen, 1997).…”

“…6), a vocal tract model is required. In our biomechanical model, the trachea is modeled as a tube and the oroesophageal cavity is modeled as a Helmholtz resonator (Riede et al, 2006;. Two equations for the tube and glottis and three linear ordinary differential equations account for the dynamics of the airflow and pressure of the vocal tract , resulting in the final output pressure.…”

“…The physical mechanism for sound production in the songbird syrinx shows analogies to that in the human larynx (Mindlin and Laje, 2005;Riede and Goller, 2010), such that both can be characterized as myoelastic-aerodynamic sound sources. This encourages the exploration of a mechanism for pressure/frequency interactions in songbirds.…”

“…Whether this mechanism, observed in a suboscine species, exists in oscine birds remains unresolved. In zebra finches (Taeniopygia guttata), there has been some evidence of correlation between air sac pressure (or vocal amplitude) and fundamental frequency (Riede et al, 2010;Ritschard and Brumm, 2011), but as the resection of the tracheosyringeal nerve resulted in large-scale disruption of acoustic features of song (e.g., see Vicario, 1991;Williams and McKibben, 1992), it has been difficult to elucidate any interplay between air sac pressure and fundamental frequency during singing.…”

Where Apes and Songbirds are Left Behind: A Comparative Assessment of the Requisites for Speech

“…Among temperate songbird species, vocalizations are generally limited to males and to contexts of territory defense and reproduction (Catchpole & Slater, 2008;Kroodsma & Miller, 1996). Male songbirds have a larger syrinx than females, despite similar body size, indicating sexual selection for more robust vocalizations (Riede, Fisher, & Goller, 2010). Further, female zebra finches, for example, have only rudimentary versions of certain song-learning and song-production telencephalon areas and produce only innate vocalization patterns (Nottebohm & Arnold, 1976).…”