Breaking symmetry: the marine environment, prey size, and the evolution of asymmetry in cetacean skulls.

Skulls of odontocetes (toothed whales, including dolphins and porpoises) are typified by directional asymmetry, particularly in elements associated with the airway. Generally, it is assumed this asymmetry is related to biosonar production. However, skull asymmetry may actually be a by-product of selection pressure for an asymmetrically positioned larynx. The odontocete larynx traverses the pharynx and is held permanently in place by a ring of muscle. This allows prey swallowing while remaining underwater without risking water entering the lungs and causing injury or death. However, protrusion of the larynx through the pharynx causes a restriction around which prey must pass to reach the stomach. The larynx and associated hyoid apparatus has, therefore, been shifted to the left to provide a larger right piriform sinus (lateral pharyngeal food channel) for swallowing larger prey items. This asymmetry is reflected in the skull, particularly the dorsal openings of the nares. It is hypothesized that there is a relationship between prey size and skull asymmetry. This relationship was examined in 13 species of odontocete cetaceans from the northeast Atlantic, including four narrow-gaped genera (Mesoplodon, Ziphius, Hyperoodon, and Kogia) and eight wide-gaped genera (Phocoena, Delphinus, Stenella, Lagenorhynchus, Tursiops, Grampus, Globicephala, and Orcinus). Skulls were examined from 183 specimens to assess asymmetry of the anterior choanae. Stomach contents were examined from 294 specimens to assess prey size. Results show there is a significant positive relationship between maximum relative prey size consumed and average asymmetry relative to skull size in odontocete species (wide-gape species: R2 = 0.642, P = 0.006; narrow-gape species: R2 = 0.909, P = 0.031). This finding provides support for the hypothesis that the directional asymmetry found in odontocete skulls is related to an aquatic adaptation enabling swallowing large, whole prey while maintaining respiratory tract protection.

The human aerodigestive tract and gastroesophageal reflux: an evolutionary perspective.

In order to appreciate fully the nature of supraesophageal complications of gastroesophageal reflux in humans, it is essential to view the problem within an evolutionary framework. Examination of the aerodigestive tract anatomy of our mammalian relatives shows that this region in humans is highly derived as compared to other mammals. Among the specializations that adult humans exhibit is a caudal position of the larynx, which results in a permanently expanded oropharynx. These anatomical features underlie our distinctive breathing and swallowing patterns and provide the substrate that allows for the production of articulate speech. While the selection factors that have shaped human evolution obviously favored our derived aerodigestive tract, aspects of this anatomy appear particularly unsuited to accommodate gastroesophageal reflux. Indeed, our unique aerodigestive tract morphology may predispose us to an array of supraesophageal complications of gastroesophageal reflux.

Anatomy of the hyoid apparatus in Odontoceti (toothed whales): specializations of their skeleton and musculature compared with those of terrestrial mammals.

BACKGROUND: The hyoid apparatus of odontocetes (toothed whales) serves as a major attachment point for many of the muscles and ligaments subserving breathing, swallowing, and sound production. METHODS: This study examines the hyoid apparatus in 48 specimens of ten odontocete genera (Phocoena, Lagenorhynchus, Stenella, Delphinus, Tursiops, Grampus, Globicephala, Mesoplodon, Physeter, and Kogia) collected post mortem from beach strandings. RESULTS: The odontocete hyoid apparatus, as that of their closest terrestrial relatives, the artiodactyls, is divisible into a basal portion (basihyal, paired thyrohyals) and a suspensory portion (paired ceratohyals, epihyals, stylohyals, and tympanohyals) connecting the basal portion to the skull base. Unlike other terrestrial mammals, the basal portion lies inferior to the laryngeal aditus, is flattened dorso-ventrally, and is relatively large, thus providing a broad surface area for muscle attachments. The suspensory elements are not as flattened and are joined by synovial joints (except for epihyal-stylohyal fusion). Muscular specializations include enlargement of those which retract the hyoid apparatus (e.g., sternohyoid) or control the tongue (e.g., styloglossus, hyoglossus). These muscles may be particularly important in a specialized prey capture behavior called suction feeding. In addition, the hyoid apparatus has a tilted placement, which allows asymmetrical enlargement of the piriform sinuses. Asymmetry is also seen in the muscular attachments between the larynx and the hyoid apparatus. The most pronounced differences from the basic pattern are observed in two families: Physeteridae and Ziphiidae. CONCLUSIONS: The derived position and shape of the odontocete hyoid apparatus may have evolved to subserve several specialized upper respiratory/digestive tract functions, such as simultaneous feeding (suction and swallowing) and sound production.

Specializations of the human upper respiratory and upper digestive systems as seen through comparative and developmental anatomy.

The human upper respiratory, or aerodigestive, tract serves as the crossroads of our breathing, swallowing and vocalizing pathways. Accordingly, developmental or evolutionary change in any of these functions will, of necessity, affect the others. Our studies have shown that the position in the neck of the mammalian larynx is a major factor in determining function in this region. Most mammals, such as our closest relatives the nonhuman primates, exhibit a larynx positioned high in the neck. This permits an intranarial larynx to be present and creates largely separate respiratory and digestive routes. While infant humans retain this basic mammalian pattern, developmental descent of the larynx considerably alters this configuration. Adult humans have, accordingly, lost separation of the respiratory and digestive routes, but have gained an increased supralaryngeal region of the pharynx which allows for the production of the varied sounds of human speech. How this region has changed during human evolution has been difficult to assess due to the absence of preserved soft-tissue structures. Our studies have shown that the relationship between basicranial shape and laryngeal position in living mammals can be a valuable guide to reconstruct the region in ancestral humans. Based on these findings we have examined the basicrania of fossil ancestors--from over two million years ago to near recent times--and have reconstructed the position of the larynx and pharyngeal region in these early forms. This has allowed us insight into how our ancestors may have breathed and swallowed, and when the anatomy necessary for human speech evolved.

Effect of basicranial flexion on larynx and hyoid position in rats: an experimental study of skull and soft tissue interactions.

The mammalian upper respiratory tract is a functionally dynamic region involved in respiration, deglutition, and phonation. As the structures of this area (e.g., larynx, hyoid) are suspended from the basicranium, changes in basicranial shape may affect both their anatomy and function. Although skeletal/soft tissue relationships have been examined through descriptive, comparative anatomy, these relationships have remained largely unexplored via experimental study. In this study, mechanical relationships between basicranial shape and positions of the larynx and hyoid bone are investigated experimentally. Skull base flexion was induced by surgically ablating the spheno-occipital synchondrosis in 13-day-old rats. Lateral radiograms were taken at 40, 60, 80, 100, and 120 days, and angular measurements made of basicranial shape and positions of the larynx and hyoid bone. Statistical analysis shows significant differences between experimental and control groups for skull base, hyoid, and larynx angles, and negative (inverse) correlations for basicranial shape change vs. hyoid position, and basicranial shape change vs. larynx position. Results show induced basicranial flexion caused inferior displacement of the larynx and hyoid bone, thus indicating a direct, mechanical relationship between skeletal and soft tissues. These observations may aid in understanding the basic biological, pathological, and evolutionary interactions of hard and soft tissues of the upper respiratory region.

A new surgical approach to the skull base in rats.

A new procedure is described to surgically approach the rat skull base and visualize the spheno-occipital synchondrosis. This region is difficult to assess in small laboratory animals without incurring damage to midline structures. This method, however, uses a lateral approach through an anterior triangle of the neck bounded by the sternocleidomastoid, digastric (posterior belly) and omohyoid muscles. No structures are transected in this procedure, thus preserving the underlying anatomy. This oblique angle of approach allows clear visualization of the mid-basicranium while sparing retraction or surgical trauma to respiratory and digestive structures such as the larynx, trachea and esophagus.

A new method for radiographically locating upper respiratory and upper digestive tract structures in rats.

A new procedure is described for radiographically locating structures of the upper respiratory and upper digestive tracts. These structures are difficult to visualize in small laboratory animals. In this method, a barium paste and tantalum dust mixture is specifically applied to the epiglottis, valleculae, soft palate and tongue in anesthetized rats to identify their positions. The mixture is easily visualized in radiograms and offers many advantages over traditional techniques, such as liquid barium swallows, insufflated tantalum powder or solid metallic implants. This enhanced visibility is due to the mixture's viscosity, which allows it to remain on the structures longer despite copious salivary flow. In addition, the thick consistency allows the radiopaque marker to adhere only where placed initially, and thus enables more precise measurements of the shape and position of upper respiratory and upper digestive tract structures.

Existence of vocal folds in the larynx of odontoceti (toothed whales).

Odontocetes (toothed whales) vocalize for communication and echolocation. The mechanisms of sound production, however, remain unclear. Their larynx has long been thought to lack vocal folds and, thus, was considered incapable of generating sounds. This study investigates internal anatomy of the odontocete larynx to: 1) describe the morphology of any folds found, 2) determine any structural homologies between these folds and the vocal folds of terrestrial mammals, and 3) assess their possible function in sound production. Larynges of 24 odontocetes representing ten genera (Delphinus, Stenella, Lagenorhynchus, Tursiops, Grampus, Delphinapterus, Globicephala, Kogia, Mesoplodon, and Phocoena) were studied post mortem. Nine specimens were cut midsagittally, and the remainder were dorsally opened to reveal internal anatomy. Results show that, contrary to established belief, vocal folds are consistently present. They are not isolated bands or "cords," but appear continuous with the internal laryngeal membrane. The attachments of these folds are the same as in terrestrial mammals, thus indicating homology with true mammalian vocal folds. These folds extend from the midline of the thyroid cartilage to the base of the arytenoid cartilages, sometimes to a discrete process. The vocal folds are elongated and oriented in a vertical plane, parallel to airflow direction. Vocal fold morphology varies, appearing as true bifurcated structures, a trifurcated fold, or a single midline fold. Laryngeal ventricles and vestibular folds are also consistently found lateral to the vocal folds. The vocal folds may divide the airstream within the larynx into three separate air currents. Fold vibrations may produce initial laryngeal sound used in echolocation or communication.

Position of the larynx in odontoceti (toothed whales).

This study examines the positional relationships of the odontocete (toothed whale) larynx to further an understanding of their breathing, swallowing, and vocalizing abilities. Seventeen specimens representing nine cetacean genera (Delphinus, Stenella, Tursiops, Grampus, Delphinapterus, Globicephala, Kogia, Mesoplodon, and Phocoena) were studied post mortem. Nine specimens were sectioned in the midsagittal plane and the position of the larynx relative to vertebral levels, skull base, and palatal structures was recorded. In eight specimens that could not be bisected for reasons of large size or condition of preservation, the larynx was removed by a ventral approach for further dissection. The results show that the upper respiratory tract of the odontocetes has evolved away from a basic mammalian pattern. Laryngeal position among terrestrial mammals usually corresponds to the level of cervical vertebrae 1-3. The odontocete larynx, however, lies rostral to the level of the atlas and extends to the presphenoidal synchondrosis. Its extension above the level of the foramen magnum is due to three factors: 1) The larynx is elongated into a tubular extension that projects beyond the soft palate into the nasopharynx; 2) the neck region is shortened owing to the highly compressed cervical vertebrae; and 3) the skull base is oriented in the same direction as the cervical vertebrae because of the horizontal and fusiform alignment of the head and thorax. Whereas the larynx of most terrestrial mammals is separable from the nasopharynx, that of the odontocetes studied may be permanently intranarial, held in place by the palatopharyngeal sphincter. Laryngeal position may affect their vocal abilities, allowing odontocetes to simultaneously swallow and echolocate.