Linear versus geometric morphometric approaches for the analysis of head shape dimorphism in lizards

Differences between the sexes may arise because of differences in reproductive strategy, with females investing more in traits related to reproductive output and males investing more in traits related to resource holding capacity and territory defence. Sexual dimorphism is widespread in lizards and in many species males and females also differ in head shape. Males typically have bigger heads than females resulting in intersexual differences in bite force. Whereas most studies documenting differences in head dimensions between sexes use linear dimensions, the use of geometric morphometrics has been advocated as more appropriate to characterize such differences. This method may allow the characterization of local shape differences that may have functional consequences, and provides unbiased indicators of shape. Here, we explore whether the two approaches provide similar results in an analyses of head shape in Tupinambis merianae. The Argentine black and white tegu differs dramatically in body size, head size, and bite force between the sexes. However, whether the intersexual differences in bite force are simply the result of differences in head size or whether more subtle modifications (e.g., in muscle insertion areas) are involved remains currently unknown. Based on the crania and mandibles of 19 lizards with known bite force, we show intersexual differences in the shape of the cranium and mandible using both linear and geometric morphometric approaches. Although both types of analyses showed generally similar results for the mandible, this was not the case for the cranium. Geometric morphometric approaches provided better insights into the underlying functional relationships between the cranium and the jaw musculature, as illustrated by shape differences in muscle insertion areas not detected using linear morphometric data. J. Morphol. 275:1016–1026, 2014. © 2014 Wiley Periodicals, Inc.     

Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats

Variation in behaviour, performance and ecology are traditionally associated with variation in morphology. A neglected part of this ecomorphological paradigm is the interaction between behaviour and performance, the ability to carry out tasks that impact fitness. Here we investigate the relationship between biting behaviour and performance (bite force) among 20 species of ecologically diverse bats. We studied the patterns of evolution of plasticity in biting behaviour and bite force, and reconstructed ancestral states for behaviour and its plasticity. Both behavioural and performance plasticity exhibited accelerating evolution over time, and periods of rapid evolution coincided with major dietary shifts from insect‐feeding to plant‐feeding. We found a significant, positive correlation between behavioural plasticity and bite force. Bats modulated their performance by changing their biting behaviour to maximize bite force when feeding on hard foods. The ancestor of phyllostomids was likely a generalist characterized by high behavioural plasticity, a condition that also evolved in specialized frugivores and potentially contributed to their diversification.     

Testing for evolutionary trade-offs in a phylogenetic context: ecological diversification and evolution of locomotor performance in emydid turtles

The evolution of ecological trade-offs is an important component of ecological specialization and adaptive radiation. However, the pattern that would show that evolutionary trade-offs have occurred between traits among species has not been clearly defined. In this paper, we propose a phylogeny-based definition of an evolutionary trade-off, and apply it to an analysis of the evolution of trade-offs in locomotor performance in emydid turtles. We quantified aquatic and terrestrial speed and endurance for up to 16 species, including aquatic, semi-terrestrial and terrestrial emydids. Emydid phylogeny was reconstructed from morphological characters and nuclear and mitochondrial DNA sequences. Surprisingly, we find that there have been no trade-offs in aquatic and terrestrial speed among species. Instead, specialization to aquatic and terrestrial habitats seems to have involved trade-offs in speed and endurance. Given that trade-offs between speed and endurance may be widespread, they may underlie specialization to different habitats in many other groups.     

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.     

Evolution of bite force in Darwin's finches: a key role for head width

Studies of Darwin's finches of the Galapagos Islands have provided pivotal insights into the interplay of ecological variation, natural selection, and morphological evolution. Here we document, across nine Darwin's finch species, correlations between morphological variation and bite force capacity. We find that bite force correlates strongly with beak depth and width but only weakly or not at all with beak length, a result that is consistent with prior demonstrations of natural selection on finch beak morphology. We also find that bite force is predicted even more strongly by head width, which exceeds all beak dimensions in predictive strength. To explain this result we suggest that head width determines the maximum size, and thus maximum force generation capacity of finch jaw adductor muscles. We suggest that head width is functionally relevant and may be a previously unrecognized locus of natural selection in these birds, because of its close relationship to bite force capacity.     

A simple morphological predictor of bite force in rodents

Bite force was quantified for 13 species of North American rodents using a piezo-resistive sensor. Most of the species measured (11) formed a tight relationship between body mass and bite force (log 10(bite force)=0.43(log 10(body mass))+0.416; R ²>0.98). This high correlation exists despite the ecological (omnivores, grazers and more carnivorous) and taxonomic (Cricetidae, Heteromyidae, Sciuridae and Zapodidae) diversity of species. Two additional species, Geomys bursarius (Geomyidae) and a Sciurus niger (Sciuridae), bit much harder for their size. We found a simple index of strength based on two measurements of the incisor at the level of the alveolus ( Z_i =((anterior-posterior length)²× (medial-lateral width))/6) that is highly predictive of bite force in these rodents (R²>0.96). Z_i may be useful for prediction of bite force (log10 (Bite Force)=0.566log10 ( Z_i )+1.432) when direct measurements are not available.     

Maximum bite force after the replacement of complete dentures

Objective: The aim of the present study was to investigate whether the maximum bite force ( MBF ) can be improved by the replacement of complete dentures for elderly people. Design: Nine edentulous volunteers, mean age 74.2 (± 5.5) years and average denture experience 19.4 ± 19.5 years (1 to 50 years) had replacement dentures made. After a rehearsal session, MBF was recorded with the old dentures, and with the new dentures immediately at insertion, at 3, 8 days, 2–3 weeks, 1, 2, 3 and 6–10 months post insertion ( p‐i. ). MBF was recorded with the central bearing point method using a full‐bridge strain gauge load cell. Data were analysed off‐line using the mean of two peak readings per patient per session. Results: The results indicate that MBF tended to be impaired when replacement dentures were first fitted (n.s.). However, this trend reversed during the first month p‐i. for patients with a “moderate” lower ridge resorption of Atwood grade 3 or 4 (n = 5). Patients with more severe lower ridge resorption Atwood grade 5 or 6 (n = 4) showed a significantly lower MBF over the entire observation period (p0.05) and took longer to regain bite strength. Only patients with moderate bone resorption exceeded their pre‐insertion level of MBF within the observation period of 6–10 months p‐i. Conclusion: The present pilot study suggests that, at least for elderly patients with severe bone resorption, delayed improvement of MBF should be expected with replacement complete dentures.     

Omnivory in lacertid lizards: adaptive evolution or constraint?

Feeding specializations such as herbivory are an often cited example of convergent and adaptive evolution. However, some groups such as lizards appear constrained in the evolution of morphological specializations associated with specialized diets. Here we examine whether the inclusion of plant matter into the diet of omnivorous lacertid lizards has resulted in morphological specializations and whether these specializations reflect biomechanical compromises as expected if omnivores are constrained by functional trade-offs. We examined external head shape, skull shape, tooth structure, intestinal tract length and bite performance as previous studies have suggested correlations between the inclusion of plants into the diet and these traits. Our data show that omnivorous lacertid lizards possess modifications of these traits that allow them to successfully exploit plant material as a food source. Conversely, few indications of a compromise phenotype could be detected, suggesting that the evolution towards herbivory is only mildly constrained by functional trade-offs.     

A new use for synchrotron X‐ray microtomography: three‐dimensional biomechanical modeling of chelicerate mouthparts and calculation of theoretical bite forces

Abstract. We present the first report on the use of the non‐invasive method of synchrotron X‐ray microtomography to model the dynamics and theoretical bite forces of arthropod mouthparts. The nature of the data allowed us to include precise measurements of muscle areas and the spatial geometry of muscle origins and insertions into a biomechanical model of a morphological microstructure. We investigated the functional morphology of the chelicera in the oribatid mite Archegozetes longisetosus (Acari, Oribatida), a model organism for Chelicerata. The chelicera represents a first‐class lever; the intrinsic muscular system consists of a feather‐shaped depressor with six muscle bundles and a bouquet‐shaped levator with 16 bundles. The relative bite forces, as compared with body mass (force/mass^2/3), are 390 N kg^?1 and lie within those known for vertebrates (≤260 N kg^?1) and decapod chelae (≤915 N kg^?1). The dynamics of force transmission and bite forces during the movement of the apotele are calculated. The conserved organization of cheliceral musculature allows broad adaptation of the model to other chelicerate taxa.     

Differential aging of bite and jump performance in virgin and mated Teleogryllus commodus crickets

Evolutionary theories of aging state that the force of natural selection declines with age, resulting in trait senescence. However, sexual selection theory predicts that costly traits that signal mate value should increase in expression as survival prospects decline. Mortality rates and fertility tend to show strong signatures of senescence, whereas sexual signaling traits increase with age, but how the expression of traits such as whole-organism performance measures that are subject to both sexual and nonsexual selection should change with age is unclear. We examined the effects of both a key life-history event (mating) and diet quality (male and female optimal diets) on aging in two whole-organism performance traits (bite force and jump take-off velocity) in male and female Teleogryllus commodus crickets. We found no evidence for diet effects on any of the measured traits. Aging effects were more evident in females than in males for both jumping and biting, and constitute a mix of senescence and terminal investment patterns depending on sex/mating class. Sex and mating therefore have important implications for resource allocation to performance traits, and hence for aging of those traits, and interactions between these two factors can result in complex changes in trait expression over individual lifetimes.     

A quantitative genetic analysis of leaf beetle larval performance on two natural hosts: including a mixed diet

Published quantitative genetic studies of larval performance on different host plants have always compared performance on one host species or genotype vs. performance on another species or genotype. The fact that some insects may feed on more than one plant species during their development has been neglected. We executed a quantitative genetic analysis of performance with larvae of the leaf beetle Oreinaelongata, raised on each of two sympatric host plants or on a mixture of them. Growth rate was higher for larvae feeding on Adenostylesalliariae, intermediate on the mixed diet and lowest on Cirsium spinosissimum. Development time was shortest on A. alliariae, intermediate on mixed diet and longest on C. spinosissimum. Survival was higher on the mixed diet than on both pure hosts. Genetic variation was present for all three performance traits but a genotype by host interaction was found only for growth rate. However, the reaction norms for growth rate are unlikely to evolve towards an optimal shape because of a lack of heritability of growth rate in each single environment. We found no negative genetic correlations for performance traits among hosts. Therefore, our results do not support a hypothesis predicting the existence of between‐host trade‐offs in performance when both hosts are sympatric with an insect population. We conclude that the evolution of host specialized genotypes is unlikely in the study population.     

Dental root size in bats with diets of different hardness

The relationship between tooth roots and diet is relatively unexplored, although a logical relationship between harder diets and increased root surface area (RSA) is suggested. This study addresses the interaction between tooth morphology, diet, and bite force in small mammals, phyllostomid bats. Using micro computed tomography (microCT), tooth root morphology of two fruit‐eating species (Carollia perspicillata and Chiroderma villosum) and two insect‐eating species (Mimon bennettii and Macrotus californicus) was compared. These species did not differ in skull or estimated body size. Food hardness, rather than dietary classification, proved to be the strongest grouping factor, with the two insectivores and the seed‐processing frugivore (C. villosum) having significantly larger RSAs. Bite force was estimated using skull measurements; bite force significantly correlated with tooth RSA but not with body size. Although the three durophagous species did exhibit larger crowns, the area of the occlusal surface did not vary among the four species. There was a linear relationship between root size and crown size, indicating that the roots were not expanded disproportionately; instead the entire tooth was larger in the hard diet species. MicroCT allows the nondestructive quantification of previously difficult‐to‐access tooth morphology; this method shows the potential for tooth roots to provide valuable dietary, behavioral, and ecological information in small mammals. J. Morphol. 276:1065–1074, 2015. © 2015 Wiley Periodicals, Inc.     

Fracture in teeth—a diagnostic for inferring bite force and tooth function

Teeth are brittle and highly susceptible to cracking. We propose that observations of such cracking can be used as a diagnostic tool for predicting bite force and inferring tooth function in living and fossil mammals. Laboratory tests on model tooth structures and extracted human teeth in simulated biting identify the principal fracture modes in enamel. Examination of museum specimens reveals the presence of similar fractures in a wide range of vertebrates, suggesting that cracks extended during ingestion or mastication. The use of ‘fracture mechanics' from materials engineering provides elegant relations for quantifying critical bite forces in terms of characteristic tooth size and enamel thickness. The role of enamel microstructure in determining how cracks initiate and propagate within the enamel (and beyond) is discussed. The picture emerges of teeth as damage‐tolerant structures, full of internal weaknesses and defects and yet able to contain the expansion of seemingly precarious cracks and fissures within the enamel shell. How the findings impact on dietary pressures forms an undercurrent of the study.     

Comparative bite forces and canine bending strength in feline and sabretooth felids: implications for predatory ecology

The sabretooth felids were widespread across much of the world in the Late Tertiary, and appear to have been an important group of large predators. Owing to the substantially different skull morphology of derived sabretooths compared with extant felids, there has been considerable debate over the killing mode, bite forces, and bending strength of the large upper canines, and over the implications of these characteristics on feeding ecology. Debates have, however, usually been based on indirect comparisons of force vectors. In this paper, I provide assessments of the estimated force output from the jaw adductor muscles, based on estimates of muscle cross-sectional areas and force vectors, along with canine bending strengths, in a variety of sabretooth felids, in comparison with extant felids. In general, sabretoothed felids had moderately powerful bites, albeit with less jaw adductor power for their body sizes compared with extant felids, sometimes markedly so. Less derived sabrecats appear to have had proportionally higher bite forces than derived forms. The length of the upper canines seemingly compromised their bending strength at any given body size, and again this was most marked in derived forms. However, compared with estimated jaw adductor forces, the canines of sabrecats appear, if anything, to have been stronger than those of extant conical-toothed felids. It has previously been suggested that large sabretoothed felids hunted large prey with a canine shearing bite, powered in part by the jaw adductors and in part by the muscles of the upper neck–occipital region. The present results of canine bending strengths versus the predicted bite force from the jaw adductors supports this suggestion.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 151 , 423–437.     

The determinants of the molecular substitution process in turtles

Neutral rates of molecular evolution vary across species, and this variation has been shown to be related to biological traits. One of the first patterns to be observed in vertebrates has been an inverse relationship between body mass (BM) and substitution rates. The effects of three major life‐history traits (LHT) that covary with BM – metabolic rate, generation time and longevity (LON) – have been invoked to explain this relationship. However, most of the theoretical and empirical evidence supporting this relationship comes from endothermic vertebrates, that is, mammals and birds, in which the environmental conditions, especially temperature, do not have a direct impact on cellular and molecular biology. We analysed the variations in mitochondrial and nuclear rates of synonymous substitution across 224 turtle species and examined their correlation with two LHT (LON and BM) and two environmental variables [latitude (LAT) and habitat]. Our analyses indicate that in turtles, neutral rates of molecular evolution are hardly correlated with LON or BM. Rather, both the mitochondrial and nuclear substitution rates are significantly correlated with LAT – faster evolution in the tropics – and especially so for aquatic species. These results question the generality of the relationships reported in mammals and birds and suggest that environmental factors might be the strongest determinants of the mutation rate in ectotherms.     

Rapid morpho‐functional changes among insular populations of the greater white‐toothed shrew

Islands are often considered to be natural laboratories where repeated ‘evolutionary experiments’ have taken place. Consequently, islands have been key model systems in our understanding of evolutionary theory. The greater white‐toothed shrew (Crocidura russula) is of interest as it has invaded French Atlantic islands within the last few thousand years and is considered to be morphologically and genetically stable in this area. In this article, we study the shape of the mandible of the greater white‐toothed shrew on four islands and compare it with that of individuals from populations on the mainland to quantify the effects of insularity. The degree of insularity (i.e. island size and distance to the continent) is thought to be linked to differences in ecological characteristics of islands compared with the mainland. We used geometric morphometric analyses to quantify differences in size and shape between populations and employed a simple biomechanical model to evaluate the potential effects of shape differences on bite force. Specimens from island populations are different from continental populations in shape and mechanical potential of the mandible. Among islands, the mandible shows various shapes that are correlated with both the distance from the coast and island area. The shape differences are located on different parts of the mandible, suggesting different ecological constraints on each island. Moreover, these shapes are linked to the ‘mechanical potential’, which is markedly different between islands. Mechanical potential has been suggested to evolve in response to prey size and or mechanical properties. In conclusion, our results show that, in spite of the relatively recent colonization of the Atlantic Islands, the mandible of C. russula possesses a distinct shape. Moreover, the shape differs among islands and is probably linked to the consumption of different prey. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Estimating maximum bite performance in Tyrannosaurus rex using multi-body dynamics

Bite mechanics and feeding behaviour in Tyrannosaurus rex are controversial. Some contend that a modest bite mechanically limited T. rex to scavenging, while others argue that high bite forces facilitated a predatory mode of life. We use dynamic musculoskeletal models to simulate maximal biting in T. rex. Models predict that adult T. rex generated sustained bite forces of 35 000-57 000 N at a single posterior tooth, by far the highest bite forces estimated for any terrestrial animal. Scaling analyses suggest that adult T. rex had a strong bite for its body size, and that bite performance increased allometrically during ontogeny. Positive allometry in bite performance during growth may have facilitated an ontogenetic change in feeding behaviour in T. rex, associated with an expansion of prey range in adults to include the largest contemporaneous animals.