Bruce A. Young

Evolution of an Arsenal Structural and Functional Diversification of the Venom System in the Advanced Snakes (Caenophidia)

Venom is a key innovation underlying the evolution of advanced snakes (Caenophidia). Despite this, very little is known about venom system structural diversification, toxin recruitment event timings, or toxin molecular evolution. A multidisciplinary approach was used to examine the diversification of the venom system and associated toxins across the full range of the ∼100 million-year-old advanced snake clade with a particular emphasis upon families that have not secondarily evolved a front-fanged venom system (∼80% of the 2500 species). Analysis of cDNA libraries revealed complex venom transcriptomes containing multiple toxin types including three finger toxins, cobra venom factor, cysteine-rich secretory protein, hyaluronidase, kallikrein, kunitz, lectin, matrix metalloprotease, phospholipase A2, snake venom metalloprotease/a disintegrin and metalloprotease, and waprin. High levels of sequence diversity were observed, including mutations in structural and functional residues, changes in cysteine spacing, and major deletions/truncations. Morphological analysis comprising gross dissection, histology, and magnetic resonance imaging also demonstrated extensive modification of the venom system architecture in non-front-fanged snakes in contrast to the conserved structure of the venom system within the independently evolved front-fanged elapid or viperid snakes. Further, a reduction in the size and complexity of the venom system was observed in species in which constriction has been secondarily evolved as the preferred method of prey capture or dietary preference has switched from live prey to eggs or to slugs/snails. Investigation of the timing of toxin recruitment events across the entire advanced snake radiation indicates that the evolution of advanced venom systems in three front-fanged lineages is associated with recruitment of new toxin types or explosive diversification of existing toxin types. These results support the role of venom as a key evolutionary innovation in the diversification of advanced snakes and identify a potential role for non-front-fanged venom toxins as a rich source for lead compounds for drug design and development.

Snake Bioacoustics: Toward a Richer Understanding of the Behavioral Ecology of Snakes

Snakes are frequently described in both popular and technical literature as either deaf or able to perceive only groundborne vibrations. Physiological studies have shown that snakes are actually most sensitive to airborne vibrations. Snakes are able to detect both airborne and groundborne vibrations using their body surface (termed somatic hearing) as well as from their inner ears. The central auditory pathways for these two modes of “hearing” remain unknown. Recent experimental evidence has shown that snakes can respond behaviorally to both airborne and groundborne vibrations. The ability of snakes to contextualize the sounds and respond with consistent predatory or defensive behaviors suggests that auditory stimuli may play a larger role in the behavioral ecology of snakes than was previously realized. Snakes produce sounds in a variety of ways, and there appear to be multiple acoustic Batesian mimicry complexes among snakes. Analyses of the proclivity for sound production and the acoustics of the sounds produced within a habitat or phylogeny specific context may provide insights into the behavioral ecology of snakes. The relatively low information content in the sounds produced by snakes suggests that these sounds are not suitable for intraspecific communication. Nevertheless, given the diversity of habitats in which snakes are found, and their dual auditory pathways, some form of intraspecific acoustic communication may exist in some species.

Evaluating Hypotheses for the Transfer of Stimulus Particles to Jacobson's Organ in Snakes

Six hypotheses for transfer mechanisms to the sensory epithelium of Jacobsons organ are presented: diffusion, capillary action, ciliary currents, pinocytotic currents, direct tongue insertion, and suction. Of these, diffusion and capillary action are rejected on theoretical grounds, and ciliary and pinocytic currents are seen as playing, at best, a secondary role. Of the two remaining hypotheses, direct insertion of the tongue and suction, experimental evidence is summarized that leads to the rejection of the direct insertion hypothesis. The stimulus transfer mechanism is hypothesized to involve the generation of suction within the lumen of Jacobsons organ and its duct. It is proposed that this suction is produced by pressure from the tongue and/or the anterior lingual processes.

Dentitional surface features in snakes (Reptilia: Serpentes)

The complexity of snake tooth morphology is more varied than has been recognized in functional, evolutionary, or taxonomic studies. We surveyed a broad sample of species across taxonomic groups to document and summarize the variation present. Our survey included a scoring of dentitional features of 1169 specimens representing 611 species of snakes on four dentiferous bones (dentary, pterygoid, palatine, maxilla). Besides presence or absence of teeth on these bones, we ranked the tooth type on each bone on the basis of a four category system: basic, furrowed, grooved, or hollow tooth. Basic teeth, without surface recesses or grooves, were the most common tooth type. Hollow teeth (fangs) were found most commonly on the maxilla and grooved teeth were often adjacent. Grooved teeth, when present, were found only on the maxilla although teeth with furrows, shallow creases in the surface enamel, were found in low numbers on the dentary, pterygoid, and palatine. Teeth exhibited further specializations, including multiple grooves, basal reinforcing ridges, development of a blade-like design, variation in the degree to which the secondary groove in hollow teeth might be in evidence, and variation in the position of the groove along the shaft of the tooth.

Landlubbers to leviathans: evolution of swimming in mosasaurine mosasaurs

Abstract Incremental stages of major evolutionary transitions within a single animal lineage are rarely observed in the fossil record. However, the extraordinarily complete sequence of well preserved material spanning the 27-Myr existence of the marine squamate subfamily Mosasaurinae provides a unique exception. By comparison with extant and extinct analogs, the tail morphology of four mosasaurine genera is examined, revealing a pattern of evolution that begins with the generalized varanoid anatomy and culminates in a high-aspect-ratio fin, similar to that of sharks. However, unlike the epicercal caudal fluke of selachians in which the tail bends dorsocaudally, derived mosasaurs develop a hypocercal tail with a ventrocaudal bend. Progressive caudal regionalization, reduced intervertebral mobility, increased tail depth due to a marked downturn of the posterior caudal segment, and the development of finlike paired appendages reveal a pattern of adaptation toward an optimized marine existence. This change in morphology reflects a transition from anguilliform or sub-carangiform locomotion to carangiform locomotion, and indicates a progressive shift from nearshore dwellers to pelagic cruisers—a change in foraging habitat independently corroborated by paleobiogeographic, stable isotope, osteohistological, and paleopathological data. Evolutionary patterns similar to those observed in mosasaurine mosasaurs are seen in other secondarily aquatically adapted amniotes, notably metriorhynchid crocodyliforms, cetaceans, and ichthyosaurs, and may be explained by developmental modularity governing the observed phenotypic expression.

Mechanics of venom expulsion in Crotalus, with special reference to the role of the fang sheath.

A combination of anatomical and experimental preparations were used to explore the function of the venom delivery system in rattlesnakes (Crotalus). The distal end of the venom duct is compressed near the point where it empties into the venom chamber, a space surrounding the fang defined by the fang sheath. Within the venom chamber, the inner fang membrane lies obliquely over the base of the fang at least partially occluding the entrance orifice. When the fang is retracted the combination of the compressed venom duct and the spatial position of the inner fang membrane serve to inhibit or block venom flow. As the fang is erected beyond approximately 60° (relative to the roof of the mouth) localized compression of the fang sheath decreases the size of the venom chamber, relieves the compressive force from the venom duct, and displaces the inner fang membrane away from the entrance orifice of the fang. Pressure recordings taken at different locations along the venom delivery system demonstrate that the venom gland produces suction during relaxation of the extrinsic glandular musculature. These findings suggest that the venom delivery system of Crotalus is both more flexible and more regulated than previously assumed. Anat Rec 264:415–426, 2001.

The buccal buckle: the functional morphology of venom spitting in cobras

SUMMARY Multiple radiations of Asiatic and African cobras have independently evolved the ability to expel their venom as a pressurized horizontal stream, a behavior commonly referred to as spitting. Though the unique fang morphology of spitting cobras is well known, the functional bases of venom spitting have received little attention. The combined results of gross and microscopic morphology, high-speed digital videography, experimental manipulations of anesthetized cobras and electromyography reveal a two-part mechanism for spitting venom. Contraction of the M. protractor pterygoideus (PP) causes displacement and deformation of the palato-maxillary arch and fang sheath; ultimately this displacement removes soft tissue barriers to venom flow that are normally present within the fang sheath. The M. adductor mandibulae externus superficialis (AMES) is activated simultaneously with the PP; the AMES increases venom pressure within the venom gland, propelling a stream of venom through the venom duct and out the fang. The displacements of the palato-maxillary arch, which form the first part of the spitting mechanism, are very similar to the motions of these bones during prey ingestion (the pterygoid walk), suggesting that venom spitting may have evolved from a specialization of prey ingestion, rather than prey capture.

Is there a direct link between the ophidian tongue and Jacobson's organ?

An analysis of the interaction between the tongue and Jacobsons organ was conducted using x-ray cinematography and two experimental procedures. The results failed to support the traditional hypothesis of a direct linkage between the tongue and Jacobsons organ since the tongue was never observed to enter the lumen of Jacobsons organ. Conversely, the results presented provide strong support for the role of elevation of the anterior lingual processes as the mechanism for stimulus transfer.

On a Flap and a Foot: Aerial Locomotion in the "Flying" Gecko, Ptychozoon kuhli

Abstract We quantified the flight trajectories of Ptychozoon kuhli dropped from distances of 300 and 825 cm and the effects of removing the cutaneous flaps and binding the feet. Analyses suggested there is a threshold speed of approximately 650 cm/sec below which the lift generated does not significantly retard acceleration of the animal or permit shallow glide angles. Removal of cutaneous flaps from specimens gliding at airspeeds below 650 cm/sec had no effect on the flight; above 650 cm/sec the presence of the cutaneous flaps significantly slowed the specimen and produced shallower glide angles. Binding of the feet eliminated all maneuverability and led to a significant increase in airspeed as well as a significant decrease in glide angle. We propose that the webbed feet of Ptychozoon play a key function in gliding and that aerial locomotion in this taxon may be more similar to “flying” treefrogs than to other reptilian gliders.

On the necessity of an archetypal concept in morphology: With special reference to the concepts of “structure” and “homology”

Morphological elements, or structures, are sorted into four categories depending on their level of anatomical isolation and the presence or absence of intrinsically identifying characteristics. These four categories are used to highlight the difficulties with the concept of structure and our ability to identify or define structures. The analysis is extended to the concept of homology through a discussion of the methodological and philosophical problems of the current concept of homology. It is argued that homology is fundamentally a similarity based concept rather than a phylogenetic concept, and a proposal is put forth to return to a comparative context for homology. It is shown that for both the concepts of structure and homology ana priori assumption of stable underlying patterns (i.e. archetypes) is essential.