Cranio‐facial remodeling in domestic dogs is associated with changes in larynx position

Abstract

The hyo-laryngeal complex is a multi-segmented structure integrating the oral and pharyngeal cavities and thus a variety of critical functions related to airway control, feeding, and vocal communication. Currently, we lack a complete understanding of how the hyoid complex, and the functions it mediates, can also be affected by changes in surrounding cranio-facial dimensions. Here, we explore these relationships in a breed of domestic dog, the Portuguese Water Dog, which is characterized by strong cranio-facial variation. We used radiographic images of the upper body and head of 55 adult males and 51 adult females to obtain detailed measures of cranio-facial variation and hyoid anatomy. Principal components analysis revealed multiple orthogonal dimensions of cranio-facial variation, some of which were associated with significant differences in larynx position: the larynx occupied a more descended position in individuals with shorter, broader faces than in those with longer, narrower faces. We then tested the possibility that caudal displacement of the larynx in brachycephalic individuals might reflect a degree of tongue crowding resulting from facial shortening and reduction of oral and pharyngeal spaces. A cadaver sample was used to obtain detailed measurements of constituent bones of the hyoid skeleton and of the tongue body, and their relationships to cranio-facial size and shape and overall body size supported the tongue-crowding hypothesis. Considering the presence of descended larynges in numerous mammalian taxa, our findings establish an important precedent for the possibility that laryngeal descent can be initiated, and even sustained, in part in response to remodeling of the face and cranium for selective pressures unrelated to vocal production. These integrated changes could also have been involved in hominin evolution, where the different laryngeal positions in modern humans compared with nonhuman primates have been traditionally linked to the evolution of speech but which are likely to be multifactorial.

Head posture impacts mammalian hyoid position and suprahyoid muscle length: implication for swallowing biomechanics

“…The magnitude of passive hyoid position change owing to IHP is comparable to active hyoid excursion during swallowing in other animals [ 18 , 21 , 23 , 66 ]. Our results on the coupling relationship between IHP and hyoid position strengthen previous results from species with a diverse range of craniofacial and hyoid skeletal morphology [ 11 , 13 – 15 ]. We suggest this is a general feature of hyoid-skull relationships in mammals, independent of clade-specific variation in skeletal or soft-tissue anatomy.…”

“…We demonstrate that changes in static hyoid position are not perfectly coupled to changes in head flexion, and the hyoid-cranium spatial relationship can vary extensively across changing head posture ( figure 3 ). In support of previous studies [ 11 , 13 – 15 ], we suggest head posture should be explicitly accounted for in comparative studies for more robust inferences on inter-individual and inter-clade disparity in resting hyoid position.…”

“…Resting hyoid position in humans and other anthropoids has long been of interest for investigating the anatomical basis of speech [4][5][6][7], and recent discoveries have uncovered new diversity of resting hyoid position across mammals more broadly [3,[8][9][10]. Interspecific variation in resting hyoid position has been postulated to reflect changes in craniomandibular and hyoid morphology [3,6,11] and carry functional implications for vocalization and swallowing biomechanics [2,8,9,12]. Nonetheless, testing these hypotheses on the form-function relationship of resting hyoid position remains challenging in a comparative framework.…”

Biomechanical and Cortical Control of Tongue Movements During Chewing and Swallowing

“…The functional significance of this variation is currently unknown (Fig. 2 ) [ 132 ], but an accumulating body of evidence suggests resting hyoid posture co-varies with hyoid morphology [ 121 ], craniomandibular morphology [ 133 ], and tongue dimensions. However, teasing apart the covariation between these traits is complicated by the fact that hyoid posture also varies within individuals as a function of head flexion, as documented in humans [ 134 ], dogs [ 133 ], horses [ 135 ], opossums [ 136 ] and probably other animal models.…”

The howl of Rancho La Brea: Comparative anatomy of modern and fossil canid hyoid bones

“…However, the canid hyoid has largely been examined in other functional contexts, such as respiration (Biewener, Soghikian, & Crompton, 1985). It has also been shown to correlate with overall skull shape in domestic dogs, with brachycephalic individuals having more descended laryngeal structures (including hyoids) than dogs with longer, narrower heads (Plotsky, Rendall, Chase, & Riede, 2016). While studies have sought to characterize the vocal repertoire of canids (e.g., Schassburger, 1993) and explored the relationship between body size and vocal tract length (Plotsky, Rendall, Riede, & Chase, 2013), no attempt has been made to relate the morphology of the hyoid apparatus to the vocal capabilities of specific species.…”