Form-function relationships underlie rapid dietary changes in a lizard.

Macroevolutionary changes such as variation in habitat use or diet are often associated with convergent, adaptive changes in morphology. However, it is still unclear how small-scale morphological variation at the population level can drive shifts in ecology such as observed at a macroevolutionary scale. Here, we address this question by investigating how variation in cranial form and feeding mechanics relate to rapid changes in diet in an insular lizard (Podarcis siculus) after experimental introduction into a new environment. We first quantified differences in the skull shape and jaw muscle architecture between the source and introduced population using three-dimensional geometric morphometrics and dissections. Next, we tested the impact of the observed variation in morphology on the mechanical performance of the masticatory system using computer-based biomechanical simulation techniques. Our results show that small differences in shape, combined with variation in muscle architecture, can result in significant differences in performance allowing access to novel trophic resources. The confrontation of these data with the already described macroevolutionary relationships between cranial form and function in these insular lizards provides insights into how selection can, over relatively short time scales, drive major changes in ecology through its impact on mechanical performance.

Broader head, stronger bite: In vivo bite forces in European eel Anguilla anguilla.

This work examined three different phenotypes of the yellow-eel stage of the European eel Anguilla anguilla, broad-heads, narrow-heads and eels with an intermediate head shape. The aim was to see whether broad-headed A. anguilla, which generally consume harder, larger prey, such as crustaceans and fish, exerted greater bite force than the narrow-headed variant, which mainly consume soft, small prey such as chironomid larvae. It was found that in 99 yellow A. anguilla, in vivo bite force of broad-heads are higher compared with narrow-heads and intermediates.

Masticatory muscle architecture in a water-rat from Australasia (Murinae, Hydromys) and its implication for the evolution of carnivory in rodents.

Murines are well known for their generalist diet, but several of them display specializations towards a carnivorous diet such as the amphibious Indo-Pacific water-rats. Despite the fact that carnivory evolved repeatedly in this group, few studies have investigated associated changes in jaw muscle anatomy and biomechanics. Here, we describe the jaw muscles and cranial anatomy of a carnivorous water-rat, Hydromys chrysogaster. The architecture of the jaw musculature of six specimens captured both on Obi and Papua were studied and described using dissections. We identified the origin and insertions of the jaw muscles, and quantified muscle mass, fiber length, physiological cross-sectional area, and muscle vectors for each muscle. Using a biomechanical model, we estimated maximum incisor and molar bite force at different gape angles. Finally, we conducted a 2D geometric morphometric analyses to compare jaw shape, mechanical potential, and diversity in lever-arm ratios for a set of 238 specimens, representative of Australo-Papuan carnivorous and omnivorous murids. Our study reveals major changes in the muscle proportions among Hydromys and its omnivorous close relative, Melomys. Hydromys was found to have large superficial masseter and temporalis muscles as well as a reduced deep masseter and zygomatico-mandibularis, highlighting major functional divergence among omnivorous and carnivorous murines. Changes in these muscles are also accompanied by changes in jaw shape and the lines of action of the muscles. A more vertically oriented masseter, reduced masseteric muscles, as well as an elongated jaw with proodont lower incisors are key features indicative of a reduced propalinality in carnivorous Hydromys. Differences in the fiber length of the masseteric muscles were also detected between Hydromys and Melomys, which highlight potential adaptations to a wide gape in Hydromys, allowing it to prey on larger animals. Using a biomechanical model, we inferred a greater bite force in Hydromys than in Melomys, implying a functional shift between omnivory and carnivory. However, Melomys has an unexpected greater bite force at large gape compared with Hydromys. Compared with omnivorous Melomys, Hydromys have a very distinctive low mandible with a well-developed coronoid process, and a reduced angular process that projects posteriorly to the ascending rami. This jaw shape, along with our mechanical potential and jaw lever ratio estimates, suggests that Hydromys has a faster jaw closing at the incisor, with a higher bite force at the level of the molars. The narrowing of the Hydromys jaw explains this higher lever advantage at the molars, which constitutes a good compromise between a wide gape, a reduced anterior masseteric mass, and long fiber lengths. Lever arms of the superficial and deep masseter are less favourable to force output of the mandible in Hydromys but more favourable to speed. Compared with the small input lever arm defined between the condyle and the angular process, the relatively longer mandible of Hydromys increases the speed at the expense of the output force. This unique combination of morphological features of the masticatory apparatus possibly has permitted Hydromys to become a highly successful amphibious predator in the Indo-Pacific region.

Is the whole more than the sum of its parts? Evolutionary trade-offs between burst and sustained locomotion in lacertid lizards.

Trade-offs arise when two functional traits impose conflicting demands on the same design trait. Consequently, excellence in one comes at the cost of performance in the other. One of the most widely studied performance trade-offs is the one between sprint speed and endurance. Although biochemical, physiological and (bio)mechanical correlates of either locomotor trait conflict with each other, results at the whole-organism level are mixed. Here, we test whether burst (speed, acceleration) and sustained locomotion (stamina) trade off at both the isolated muscle and whole-organism level among 17 species of lacertid lizards. In addition, we test for a mechanical link between the organismal and muscular (power output, fatigue resistance) performance traits. We find weak evidence for a trade-off between burst and sustained locomotion at the whole-organism level; however, there is a significant trade-off between muscle power output and fatigue resistance in the isolated muscle level. Variation in whole-animal sprint speed can be convincingly explained by variation in muscular power output. The variation in locomotor stamina at the whole-organism level does not relate to the variation in muscle fatigue resistance, suggesting that whole-organism stamina depends not only on muscle contractile performance but probably also on the performance of the circulatory and respiratory systems.

Darwin's finches and their diet niches: the sympatric coexistence of imperfect generalists.

Adaptive radiation can be strongly influenced by interspecific competition for resources, which can lead to diverse outcomes ranging from competitive exclusion to character displacement. In each case, sympatric species are expected to evolve into distinct ecological niches, such as different food types, yet this expectation is not always met when such species are examined in nature. The most common hypotheses to account for the coexistence of species with substantial diet overlap rest on temporal variation in niches (often diets). Yet spatial variation in niche overlap might also be important, pointing to the need for spatiotemporal analyses of diet and diet overlap between closely related species persisting in sympatry. We here perform such an analysis by characterizing the diets of, and diet overlap among, four sympatric Darwin's ground finch species at three sites and over 5 years on a single Galápagos island (Santa Cruz). We find that the different species have broadly similar and overlapping diets - they are to some extent generalists and opportunists - yet we also find that each species retains some 'private' resources for which their morphologies are best suited. Importantly, use of these private resources increased considerably, and diet overlap decreased accordingly, when the availability of preferred shared foods, such as arthropods, was reduced during drought conditions. Spatial variation in food resources was also important. These results together suggest that the ground finches are 'imperfect generalists' that use overlapping resources under benign conditions (in space or time), but then retreat to resources for which they are best adapted during periods of food limitation. These conditions likely promote local and regional coexistence.

Isotopic and anatomical evidence of an herbivorous diet in the Early Tertiary giant bird Gastornis. implications for the structure of Paleocene terrestrial ecosystems.

The mode of life of the early Tertiary giant bird Gastornis has long been a matter of controversy. Although it has often been reconstructed as an apex predator feeding on small mammals, according to other interpretations, it was in fact a large herbivore. To determine the diet of this bird, we analyze here the carbon isotope composition of the bone apatite from Gastornis and contemporaneous herbivorous mammals. Based on (13)C-enrichment measured between carbonate and diet of carnivorous and herbivorous modern birds, the carbonate δ(13)C values of Gastornis bone remains, recovered from four Paleocene and Eocene French localities, indicate that this bird fed on plants. This is confirmed by a morphofunctional study showing that the reconstructed jaw musculature of Gastornis was similar to that of living herbivorous birds and unlike that of carnivorous forms. The herbivorous Gastornis was the largest terrestrial tetrapod in the Paleocene biota of Europe, unlike the situation in North America and Asia, where Gastornis is first recorded in the early Eocene, and the largest Paleocene animals were herbivorous mammals. The structure of the Paleocene terrestrial ecosystems of Europe may have been similar to that of some large islands, notably Madagascar, prior to the arrival of humans.

Scaling and shear transformations capture beak shape variation in Darwin's finches.

Evolution by natural selection has resulted in a remarkable diversity of organism morphologies that has long fascinated scientists and served to establish the first relations among species. Despite the essential role of morphology as a phenotype of species, there is not yet a formal, mathematical scheme to quantify morphological phenotype and relate it to both the genotype and the underlying developmental genetics. Herein we demonstrate that the morphological diversity in the beaks of Darwin's Finches is quantitatively accounted for by the mathematical group of affine transformations. Specifically, we show that all beak shapes of Ground Finches (genus Geospiza) are related by scaling transformations (a subgroup of the affine group), and the same relationship holds true for all the beak shapes of Tree, Cocos, and Warbler Finches (three distinct genera). This analysis shows that the beak shapes within each of these groups differ only by their scales, such as length and depth, which are genetically controlled by Bmp4 and Calmodulin. By measuring Bmp4 expression in the beak primordia of the species in the genus Geospiza, we provide a quantitative map between beak morphology and the expression levels of Bmp4. The complete morphological variation within the beaks of Darwin's finches can be explained by extending the scaling transformations to the entire affine group, by including shear transformations. Altogether our results suggest that the mathematical theory of groups can help decode morphological variation, and points to a potentially hierarchical structure of morphological diversity and the underlying developmental processes.

Head shape evolution in Gymnophthalmidae: does habitat use constrain the evolution of cranial design in fossorial lizards?

Habitat usage comprises interactions between ecological parameters and organismal capacities, and the selective pressures that ultimately determine the outcome of such processes in an evolutionary scale may be conflicting when the same morphological structure is recruited for different activities. Here, we investigate the roles of diet and locomotion in the evolution of cranial design in gymnophthalmid lizards and test the hypothesis that microhabitat use drives head shape evolution, particularly in head-first burrowers. Morphological factors were analysed in relation to continuous ecological indexes (prey hardness and substrate compactness) using conventional and phylogenetic approaches. Results suggest that the evolution of head morphology in Gymnophthalmidae was shaped under the influence of microhabitat use rather than diet: burrowers have shorter heads with lower rostral angulation, independently of the prey consumed. Food preferences appear to be relatively conserved throughout the phylogeny of the group, which may have permitted the extensive radiation of gymnophthalmids into fossorial microhabitats.

Why the long face? A comparative study of feeding kinematics of two pipefishes with different snout lengths.

This study showed that the mouth of Doryrhamphus dactyliophorus, a species with a relatively long snout, travels a greater distance compared with Doryrhamphus melanopleura, a species with a considerably shorter snout, allowing it to strike at prey that are farther away from the mouth. The long-snouted species also tended to reach significantly higher linear velocities of the mouth approaching the prey. On the other hand, D. melanopleura needed less time to capture its prey. A striking difference in prey-capture success was observed between species: D. melanopleura and D. dactyliophorus had a prey-capture success of 91 and 31%, respectively. The small prey size and the relatively large distance between eyes and prey are potential reasons why directing the mouth accurately to the prey is difficult in D. dactyliophorus, hence possibly explaining the lower prey-capture success in this long-snouted species.

The relationship between bite force, morphology, and diet in southern African agamids.

BACKGROUND: Many animals display morphological and behavioural adaptations to the habitats in which they live and the resources they exploit. Bite force is an important whole-organism performance trait that allows an increase in dietary breadth, the inclusion of novel prey in the diet, territory and predatory defence, and is important during mating in many lizards. METHODS: Here, we study six species of southern African agamid lizards from three habitat types (ground-dwelling, rock-dwelling, and arboreal) to investigate whether habitat use constrains head morphology and bite performance. We further tested whether bite force and head morphology evolve as adaptations to diet by analysing a subset of these species for which diet data were available. RESULTS: Overall, both jaw length and its out-lever are excellent predictors of bite performance across all six species. Rock-dwelling species have a flatter head relative to their size than other species, possibly as an adaptation for crevice use. However, even when correcting for jaw length and jaw out-lever length, rock-dwelling species bite harder than ground-dwelling species. Diet analyses demonstrate that body and head size are not directly related to diet, although greater in-levers for jaw closing (positively related to bite force) are associated to an increase of hard prey in the diet. Ground-dwelling species consume more ants than other species. CONCLUSIONS: Our results illustrate the role of head morphology in driving bite force and demonstrate how habitat use impacts head morphology but not bite force in these agamids. Although diet is associated with variation in head morphology it is only partially responsible for the observed differences in morphology and performance.

Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (Podarcis melisellensis).

If alternative phenotypes in polymorphic populations do not mate randomly, they can be used as model systems to study adaptive diversification and possibly the early stages of sympatric speciation. In this case, non random mating is expected to support genetic divergence among the different phenotypes. In the present study, we use population genetic analyses to test putatively neutral genetic divergence (of microsatellite loci) among three colour morphs of the lizard Podarcis melisellensis, which is associated with differences in male morphology, performance and behaviour. We found weak evidence of genetic divergence, indicating that gene flow is somewhat restricted among morphs and suggesting possible adaptive diversification.

Chewing variation in lepidosaurs and primates.

Mammals chew more rhythmically than lepidosaurs. The research presented here evaluated possible reasons for this difference in relation to differences between lepidosaurs and mammals in sensorimotor systems. Variance in the absolute and relative durations of the phases of the gape cycle was calculated from kinematic data from four species of primates and eight species of lepidosaurs. The primates exhibit less variance in the duration of the gape cycle than in the durations of the four phases making up the gape cycle. This suggests that increases in the durations of some gape cycle phases are accompanied by decreases in others. Similar effects are much less pronounced in the lepidosaurs. In addition, the primates show isometric changes in gape cycle phase durations, i.e. the relative durations of the phases of the gape cycle change little with increasing cycle time. In contrast, in the lepidosaurs variance in total gape cycle duration is associated with increases in the proportion of the cycle made up by the slow open phase. We hypothesize that in mammals the central nervous system includes a representation of the optimal chew cycle duration maintained using afferent feedback about the ongoing state of the chew cycle. The differences between lepidosaurs and primates do not lie in the nature of the sensory information collected and its feedback to the feeding system, but rather the processing of that information by the CNS and its use feed-forward for modulating jaw movements and gape cycle phase durations during chewing.

What determines dewlap diversity in Anolis lizards? An among-island comparison.

Animal signalling systems are extremely diverse as they are under different, often conflicting, selective pressures. A classic textbook example of a diverse signal is the anoline dewlap. Both at the inter- and intraspecific levels, dewlap size, colour, shape and pattern vary extensively. Here, we attempt to elucidate the various factors explaining the diversity in dewlap size and pattern among seven Anolis sagrei populations from different islands in the Bahamas. The seven islands differ in the surface area, number and kind of predators, sexual size dimorphism and Anolis species composition. In addition, we investigate whether selective pressures acting on dewlap design differ between males and females. Whereas dewlap pattern appears to serve a role in species recognition in both sexes, our data suggest that relative dewlap size is under natural and/or sexual selection. We find evidence for the role of the dewlap as a pursuit-deterrence signal in both males and females as relative dewlap size is larger on islands where A. sagrei occurs sympatrically with predatory Leiocephalus lizards. Additionally, in males relatively large dewlaps seem to be selected for in a sexual context, whereas in females natural selection, for instance by other predators than Leiocephalus lizards, appears to constrain relative dewlap size.

Convergence in trophic morphology and feeding performance among piscivorous natricine snakes.

Piscivory has independently evolved numerous times amongst snakes, and therefore these animals provide a powerful opportunity to test for convergent evolution in a vertebrate feeding system. In this study, we integrate performance trials with comparative methods to test the hypothesis that piscivory drives convergence in trophic morphology and feeding performance among natricine snakes. Within and across species, increasing the relative length of the quadrate bone in the skull is positively and strongly linked to a reduction in the time needed to swallow large fish prey. Thus, our feeding experiments suggest that a longer quadrate bone enables snakes to better conform their head shape to the shape of the prey during swallowing. Ancestral diet reconstructions and phylogenetically corrected multiple regression analyses further reveal that evolutionary increases in piscivory are coupled to the evolution of relatively longer quadrates, and hence improved feeding performance on fish prey in these animals. The exploitation of similar dietary niches drives the evolution of convergent trophic morphologies and feeding performances in natricine snakes.

Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis.

Species with alternative phenotypes offer unique opportunities to investigate hormone-behavior relationships. We investigated the relationships between testosterone, corticosterone, morphology, performance, and immunity in a population of lizards (Podarcis melisellensis) which exhibits a color polymorphism. Males occur in three different color morphs (white, yellow, orange), providing an opportunity to test the idea of morphs being alternative solutions to the evolutionary challenges posed on the link between hormones, morphology, performance, and immunity. Morphs differed in bite force capacity, with orange males biting harder, and in corticosterone levels, with yellow males having lower levels than orange. However, morphs did not differ in testosterone levels or in the immunological parameters tested. At the individual level, across morphs, testosterone levels predicted size-corrected bite force capacity, but no relation was found between hormone levels and immunity. Our results do not support the testosterone-based polymorphism hypothesis and reject the hypothesis of a trade-off between testosterone and immunity in this species, but provide a mechanistic link between testosterone and a sexually selected performance trait.

Head shape evolution in Tropidurinae lizards: does locomotion constrain diet?

Different components of complex integrated systems may be specialized for different functions, and thus the selective pressures acting on the system as a whole may be conflicting and can ultimately constrain organismal performance and evolution. The vertebrate cranial system is one of the most striking examples of a complex system with several possible functions, being associated to activities as different as locomotion, prey capture, display and defensive behaviours. Therefore, selective pressures on the cranial system as a whole are possibly complex and may be conflicting. The present study focuses on the influence of potentially conflicting selective pressures (diet vs. locomotion) on the evolution of head shape in Tropidurinae lizards. For example, the expected adaptations leading to flat heads and bodies in species living on vertical structures may conflict with the need for improved bite performance associated with the inclusion of hard or tough prey into the diet, a common phenomenon in Tropidurinae lizards. Body size and six variables describing head shape were quantified in preserved specimens of 23 species, and information on diet and substrate usage was obtained from the literature. No phylogenetic signal was observed in the morphological data at any branch length tested, suggesting adaptive evolution of head shape in Tropidurinae. This pattern was confirmed by both factor analysis and independent contrast analysis, which suggested adaptive co-variation between the head shape and the inclusion of hard prey into the diet. In contrast to our expectations, habitat use did not constrain or drive head shape evolution in the group.

Morphological convergence as a consequence of extreme functional demands: examples from the feeding system of natricine snakes.

Despite repeated acquisitions of aquatic or semi-aquatic lifestyles revolving around piscivory, snakes have not evolved suction feeding. Instead, snakes use frontally or laterally directed strikes to capture prey under water. If the aquatic medium constrains strike performance because of its physical properties, we predict morphological and functional convergence in snakes that use similar strike behaviours. Here we use natricine snakes to test for such patterns of convergence in morphology and function. Our data show that frontal strikers have converged on a similar morphology characterized by narrow elongate heads with a reduced projected frontal surface area. Moreover, simple computational fluid dynamics models show that the observed morphological differences are likely biologically relevant as they affect the flow of water around the head. In general, our data suggest that the direction of evolution may be predictable if constraints are strong and evolutionary solutions limited.

Kinematics of intraoral transport and swallowing in the herbivorous lizard uromastix acanthinurus

The kinematics of intraoral transport and swallowing in lizards of the species Uromastix acanthinurus (Chamaeleonidae, Leiolepidinae) were investigated using cineradiography (50 frames s-1). Additional recordings were also made using high-speed (500 frames s-1) and conventional video systems (25 frames s-1). Small metal markers were inserted into different parts of the upper and lower jaw and the tongue. Cineradiographic images were digitised, and displacements of the body, head, upper and lower jaw and the tongue were quantified. Twenty additional variables depicting displacements and the timing of events were calculated. Multivariate analyses of variance indicated significant differences between feeding stages. Remarkably, only very few food-type-dependent differences were observed during intraoral transport, and no such differences could be demonstrated during swallowing. Using previously published data for the closely related insectivorous lizard Plocederma stellio, the effect of dietary specialisation in U. acanthinurus on the kinematic variables while eating locusts was examined. Species differed in a number of gape- and tongue-related variables. These differences may be related to differences in tongue structure between the species. Clearly, U. acanthinurus possesses a specialised gut and dental structure that allows them efficiently to cut pieces from whole leaves. However, a decrease in modulatory capacity seems to be a consequence of dietary specialisation in Uromastix acanthinurus.

Quantitative analysis of jaw and hyolingual muscle activity during feeding in the lizard Agama stellio

The activity of jaw and hyolingual muscles during the entire feeding sequence is examined in the lizard Agama stellio, with special focus on the intraoral transport and swallowing stages. Correlation of electromyography (EMG) data with kinematics shows that the kinematic phases (slow opening, SO; fast opening, FO; fast closing, FC; slow closing/power stroke, SC/PS) are characterised by distinct activities in the jaw and hyolingual muscles. The SO phase is clearly the result of tongue protraction (upon protraction, the tongue is pulled against the prey and consequently the lower jaw is pushed down), whereas the FO phase is caused by activity in the jaw opener and dorsal cervical muscles. Both the FC and SC/PS phases are characterised by pronounced activity in the jaw adductor muscles. Tongue retraction is produced by activity in the hyoid and tongue retractor muscles. A quantitative analysis of time-related EMG data shows that, in accordance with the kinematic analyses, three different stages can be recognised as components of the feeding cycle: prey capture, intraoral transport and swallowing. However, analysis of intensity-related data allowed a fourth stage, crushing, to be detected. Whereas there are indications that prey capture, intraoral transport and swallowing are controlled by different motor patterns, the differences between crushing and transport are likely to be caused by feedback mechanisms. Our results show the importance of including intensity-related data in quantitative analyses of EMG recordings in order to discriminate between feeding stages. Additionally, it is shown that both the jaw and the hyolingual muscles play crucial roles during feeding. During all stages, movements of the hyolingual apparatus are an essential part of the feeding cycle. Thus, when examining lizard feeding mechanisms, the activity patterns of the hyolingual muscles should not be neglected.

Kinematics of feeding in the lizard Agama stellio

The kinematics of prey capture, intraoral transport and swallowing in lizards of the species Agama stellio (Agamidae) were investigated using cineradiography (50 frames s-1) and high-speed video recordings (500 frames s-1). Small metal markers were inserted into different parts of the upper and lower jaw and the tongue. Video and cineradiographic images were digitized, and displacements of the body, head, upper and lower jaw and the tongue were quantified. Twenty additional variables depicting displacements and timing of events were calculated. A factor analysis performed on the kinematic data separates prey capture and swallowing cycles from intraoral transport bites. However, the intraoral transport stage cannot be separated into chewing (reduction) and transport bites. The effect of prey type and size on the feeding kinematics of intraoral transport and swallowing cycles was investigated. During the intraoral transport stage, distinct aspects (e.g. durations, maximal excursions) of the gape and tongue cycle are modulated in response to both the size and type of the prey item. The results for A. stellio generally agree with a previous model, although it is the entire slow opening phase rather than solely the duration of the second part of this phase that is affected by the size of the prey. The intraoral transport cycles in A. stellio show the two synapomorphic characteristics of tetrapods (tongue-based terrestrial intraoral prey transport and the existence of a long preparatory period of prey compression). However, not all five characters of the feeding cycle previously proposed for amniotes are present in A. stellio. One major difference is that in A. stellio the recovery of the hyolingual apparatus does not take place during the slow opening phase but during the slow closing/powerstroke phase.