The evolution of bite force in horned lizards: the influence of dietary specialization.

Dietary specialization is an important driver of the morphology and performance of the feeding system in many organisms, yet the evolution of phenotypic specialization has only rarely been examined within a species complex. Horned lizards are considered primarily myrmecophagous (ant eating), but variation in diet among the 17 species of horned lizards (Phrynosoma) makes them an ideal group to examine the relationship between dietary specialization and the resultant morphological and functional changes of the feeding system. In this study, we perform a detailed analysis of the jaw adductor musculature and use a biomechanical model validated with in vivo bite force data to examine the evolution of bite force in Phrynosoma. Our model simulations demonstrate that bite force varies predictably with respect to the gape angle and bite position along the tooth row, with maximal bite forces being attained at lower gape angles and at the posterior tooth positions. Maximal bite forces vary considerably among horned lizards, with highly myrmecophagous species exhibiting very low bite forces. In contrast, members of the short-horned lizard clade are able to bite considerably harder than even closely related dietary generalists. This group appears to be built for performing crushing bites and may represent a divergent morphology adapted for eating hard prey items. The evolutionary loss of processing morphology (teeth, jaw and muscle reduction) and bite force in ant specialists may be a response to the lack of prey processing rather than a functional adaptation per se.

Directional evolution of stockiness coevolves with ecology and locomotion in lizards.

Although studied in many taxa, directional macroevolution remains difficult to detect and quantify. We present an approach for detecting directional evolution in subclades of species when relatively few species are sampled, and apply it to studying the evolution of stockiness in Phrynosomatine lizards. Our approach is more sensitive to detecting the tempo of directional evolution than other available approaches. We use ancestral reconstruction and phylogenetic mapping of morphology to characterize the direction and magnitude of trait evolution. We demonstrate a directional trend toward stockiness in horned lizards, but not their sister groups, finding that stockier species tend to have relatively short and wide bodies, and relatively short heads, tails, and limbs. Ornstein-Uhlenbeck models show that the directional trend in horned lizards is due to a shift in selective regime and stabilizing selection as opposed to directional selection. Bayesian evolutionary correlation analyses indicate that stockier species run more slowly and eat a larger proportion of ants. Furthermore, species with larger horns tend to be slower and more ant-specialized. Directional evolution toward a stocky body shape has evolved in conjunction with changes in a suite of traits, representing a complex example of directional macroevolution.

Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis).

The evolutionary processes that result in reliable links between male signals and fighting capacity have received a great deal of attention, but the proximate mechanisms underlying such connections remain understudied. We studied a large sample of male green anole lizards (Anolis carolinensis) to determine whether testosterone or corticosterone predicted dewlap size and/or bite-force capacity, as dewlap size is known to be a reliable predictor of bite-force capacity in territorial males. We also examined whether these relationships were consistent between previously described body size classes ("lightweights" and "heavyweights"). Heavyweights had 50% higher testosterone concentrations than lightweights during the breeding season, suggesting a mechanism for the disproportionately larger heads and dewlaps and higher bite-forces of heavyweights. Plasma testosterone concentrations were positively correlated with dewlap size and bite-force performance in lightweights (but not heavyweights) but only because of mutual intercorrelation of all three variables with body size. We suggest two possibilities for the relationship between testosterone levels and body size: (1) testosterone promotes growth in this species or (2) smaller sexually mature males are unable to compete with larger males such that the benefits of elevated testosterone do not outweigh the costs. Corticosterone levels did not differ between the male morphs, and lightweights, but not heavyweights, showed an inverse relationship between testosterone levels and corticosterone levels. Our results suggest that testosterone is important for traits related to dominance in adult male green anoles and may influence the ability to compete with rivals via fighting ability or through the use of signals.

Modulation of prey capture kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps.

Most organisms feed on a variety of prey that may differ dramatically in their physical and behavioural characteristics (e.g. mobility, mass, texture, etc.). Thus the ability to modulate prey capture behaviour in accordance with the characteristics of the food appears crucial. In animals that use rapid tongue movements to capture prey (frogs and chameleons), the coordination of jaws and tongue is based on visual cues gathered prior to the prey capture event. However, most iguanian lizards have much slower tongue-based prey capture systems suggesting that sensory feedback from the tongue may play an important role in coordinating jaw and tongue movements. We investigated the modulation of prey capture kinematics in the agamid lizard Pogona vitticeps when feeding on a range of food items differing in their physical characteristics. As the lizard is a dietary generalist, we expected it to be able to modulate its prey capture kinematics as a function of the (mechanical) demands imposed by the prey. Additionally, we investigated the role of lingual sensory feedback by transecting the trigeminal sensory afferents. Our findings demonstrated that P. vitticeps modulates its prey capture kinematics according to specific prey properties (e.g. size). In addition, transection of the trigeminal sensory nerves had a strong effect on prey capture kinematics. However, significant prey type effects and prey type by transection effects suggest that other sources of sensory information are also used to modulate the prey capture kinematics in P. vitticeps.

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace.

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.

The evolution of cranial design and performance in squamates: Consequences of skull-bone reduction on feeding behavior.

The evolution of cranial design in lepidosaurians is characterized by a general trend toward the loss of cranial elements. The evolution of relatively lighter skulls in squamates appears tightly coupled to a reduction in relative mass of the jaw adductor, implying functional consequences for bite force and feeding behavior. Interestingly, among squamates the postorbital bar was reduced or lost at least twice independently and taxa characterized by the loss of these cranial elements (e.g., geckos and varanids) are generally reported as having a mobile skull. In Gekkotans, the loss of the postorbital bar was accompanied by a reduction of the supratemporal bar, resulting in a pronounced cranial kinesis. Our data show that having a kinetic skull has functional consequences and results in a reduction in bite force. The lower bite force may in turn be responsible for the decreased feeding efficiency as reflected in the longer duration of intra-oral transport cycles. Gekkotans, however, appear to exploit their intracranial mobility in ways that increases the velocity of jaw movement during opening and closing, which may allow them to capture more elusive prey. The morphological changes observed in the evolution of the cranial system in squamates appear tightly linked to functional and constructional demands on the skull, making squamate skull evolution a model system to investigate the consequences of morphological changes in a complex integrated system of performance, behavior, and ecology.

Prey capture kinematics of ant-eating lizards.

While morphological and behavioral feeding specializations are obvious in many vertebrate groups, among lizards there appear to be few dietary specialists. By comparing the prey capture kinematics and overall feeding behavior in two highly specialized ant-eating lizards (Moloch horridus and Phrynosoma platyrhinos) with those of two closely related dietary generalists (Pogona vitticeps and Uma notata), we investigate whether dietary specialization has been accompanied by changes in the function and use of the feeding system. We quantified kinematic variables from high-speed video recordings (200-250 frames s(-1)) of each species feeding on ants. Prey capture was strikingly different in M. horridus to that of other species, being characterized by a suite of unusual behaviors including the lack of a body lunge, faster tongue protrusion, reduced prey processing and, most notably, the ability to modulate the slow open phase of the gape cycle. In concert, these traits make a single feeding event in M. horridus faster than that in any other iguanian lizard studied to date. Prey capture behavior in P. platyrhinos is kinematically more similar to U. notata and P. vitticeps than to M. horridus, but the ant specialists are similar in that both lack distinct prey processing behaviors, resulting in faster overall capture and feeding events. While ant feeding in P. vitticeps is faster than feeding on other prey, the duration of a single feeding event is still four times longer than in either ant specialist, because of extensive prey processing. Additionally, a phylogenetic comparison of ant specialist lizards with dietary generalists revealed that ant-eating lizards require significantly less time to capture and process prey. Thus there are not only significant behavioral modifications in these ant-eating lizards, but also multiple strategies among specialists, suggesting differing selective pressures or phylogenetic constraints in the evolution of ant eating in lizards.

Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis).

The evolution of alternative male phenotypes is probably driven by male-male competition for access to reproductive females, but few studies have examined whether whole-organism performance capacities differ between male morphs, and if so whether any such differences affect fighting ability. We show how ontogenetic changes in performance and morphology have given rise to two distinct life-stage male morphs exhibiting different fighting tactics within the green anole lizard (Anolis carolinensis). Field studies show a bimodal distribution of adult males within a single population: larger 'heavyweight' males have relatively large heads and high bite forces for their size, whereas smaller 'lightweight' males have smaller heads and lower bite forces. In staged fights between size-matched heavyweight males, males with greater biting ability won more frequently, whereas in lightweight fights, males with greater jumping velocity and acceleration won more often. Because growth in reptiles is indeterminate, and the anole males examined are sexually mature, we propose that the heavyweight morph arose through selection against males with small heads and poor bite forces at the lightweight-heavyweight size transition. Our findings imply that one may not be able to predict male fighting success (and hence potential mating success) by examining aspects of male 'quality' at only one life stage.

Mechanism of tongue protraction in microhylid frogs.

High-speed videography and muscle denervation experiments were used to elucidate the mechanism of tongue protraction in the microhylid frog Phrynomantis bifasciatus. Unlike most frogs, Phrynomantis has the ability to protract the tongue through a lateral arc of over 200 degrees in the frontal plane. Thus, the tongue can be aimed side to side, independently of head and jaw movements. Denervation experiments demonstrate that the m. genioglossus complex controls lateral tongue aiming with a hydrostatic mechanism. After unilateral denervation of the m. genioglossus complex, the tongue can only be protracted towards the denervated (inactive) side and the range through which the tongue can be aimed is reduced by 75%. Histological sections of the tongue reveal a compartment of perpendicularly arranged muscle fibers, the m. genioglossus dorsoventralis. This compartment, in conjunction with the surrounding connective tissue, generates hydrostatic pressure that powers tongue movements in Phrynomantis. A survey of aiming abilities in 17 additional species of microhylid frogs, representing a total of 12 genera and six subfamilies, indicates that hydrostatic tongues are found throughout this family. Among frogs, this mechanism of tongue protraction was previously known only in Hemisus and may represent a synapomorphy of Hemisus and Microhylidae.

Supercontracting muscle: producing tension over extreme muscle lengths.

Muscle mechanics dictates a trade-off between the ability of a muscle to generate isometric force and its length. This intrinsic trade-off is the result of the need for overlap between thick and thin filaments upon extension of the sarcomere and of the limitations imposed by the physical interference between the thin filaments and the thick filaments with the Z-disk upon contraction. However, previously published data indicate that chameleons are able to produce a nearly constant tongue retraction force over a wide range of tongue extension lengths, made possible by the presence of supercontracting muscle in the tongue retractors. Investigation of the length/tension properties and ultrastructure of the tongue retractor in a closely related agamid lizard (Pogona vitticeps) indicates that the ability to generate tension at extreme elongation is probably a derived feature for chameleons. Whereas chameleons are unique among vertebrates in possessing supercontracting muscle, this seems to be a common phenomenon in invertebrates. However, the presence of supercontracting muscle in chameleons and in several invertebrate groups seems to be coupled to the need to generate tension over large changes in muscle length and might be a more general solution for this problem.

Comparative study of the innervation patterns of the hyobranchial musculature in three iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus, and Chamaeleo jacksonii.

The neuroanatomy and musculature of the hyobranchial system was studied in three species of iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus, and Chamaeleo jacksonii. The goal of this study was to describe and compare the innervation and arrangement of the hyobranchial musculature in the context of its function during tongue protrusion. A comparison of the hyobranchial innervation patterns revealed a relatively conserved innervation pattern in S. undulatus and P. sinaitus, and a modified version of this basic layout in C. jacksonii. All three species show anastomoses between sensory neurons of the trigeminal nerve and motor neurons of the hypoglossal nerve, suggesting that feedback may be important in coordinating tongue, jaw, and hyoid movements. The hyobranchial musculature of S. undulatus is very similar to that of P. sinaitus; however, there are minor differences, including the presence of an M. genioglossus internus (GGI) muscle in S. undulatus. Further differences are found mainly in functional aspects of the hyobranchial musculature, such as changes in the muscle lengths and the origins and insertions of the muscles. In C. jacksonii the hyobranchial system is comprised of largely the same components, but it has become highly modified compared to the other two species. Based on the innervation and morphological data gathered here, we propose a revision of the terminology for the hyobranchial musculature in iguanian lizards.