Evolution of extreme body size disparity in monitor lizards (Varanus)

Many features of species' biology, including life history, physiology, morphology, and ecology are tightly linked to body size. Investigation into the causes of size divergence is therefore critical to understanding the factors shaping phenotypic diversity within clades. In this study, we examined size evolution in monitor lizards (Varanus), a clade that includes the largest extant lizard species, the Komodo dragon (V. komodoensis), as well as diminutive species that are nearly four orders of magnitude smaller in adult body mass. We demonstrate that the remarkable body size disparity of this clade is a consequence of different selective demands imposed by three major habitat use patterns-arboreality, terrestriality, and rock-dwelling. We reconstructed phylogenetic relationships and ancestral habitat use and applied model selection to determine that the best-fitting evolutionary models for species' adult size are those that infer oppositely directed adaptive evolution associated with terrestriality and rock-dwelling, with terrestrial lineages evolving extremely large size and rock-dwellers becoming very small. We also show that habitat use affects the evolution of several ecologically important morphological traits independently of body size divergence. These results suggest that habitat use exerts a strong, multidimensional influence on the evolution of morphological size and shape disparity in monitor lizards.     

Diversification of body shape in Sebastes rockfishes of the north‐east Pacific

Body shape variation is integrally related to many aspects of fish ecology, including locomotion and foraging, and can indicate the functional diversity of fish assemblages. Few studies have thoroughly characterized body shape in a diverse marine fish clade, or investigated both temporal and spatial patterns of variation in body shape disparity. Here, I use digital photographs to measure geometric body shape in 66 species of north‐east Pacific rockfish (Sebastes spp.), including a correction for error introduced by arching of specimens. Different components of interspecific shape variation show associations with fish size, depth habitat, trophic niche and phylogenetic relationships. Overall, the accumulation of body shape disparity appears to have been near‐constant over time, and shows little variation across the latitudinal range of rockfish.     

Convergence and the multidimensional niche

Convergent evolution has played an important role in the development of the ecological niche concept. We investigated patterns of convergent and divergent evolution of Caribbean Anolis lizards. These lizards diversified independently on each of the islands of the Greater Antilles, producing the same set of habitat specialists on each island. Using a phylogenetic comparative framework, we examined patterns of morphological convergence in five functionally distinct sets of morphological characters: body size, body shape, head shape, lamella number, and sexual size dimorphism. We find evidence for convergence among members of the habitat specialist types for each of these five datasets. Furthermore, the patterns of convergence differ among at least four of the five datasets; habitat specialists that are similar for one set of characters are often greatly different for another. This suggests that the habitat specialist niches into which these anoles have evolved are multidimensional, involving several distinct and independent aspects of morphology.     

The influence of size on body shape diversification across Indo‐Pacific shore fishes*

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo‐Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage‐specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.     

Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards

Understanding the relationship between form and function is central to our comprehension of how phenotypic diversity evolves. Traits involved in multiple activities, such as social interactions and ecological resource use, are under the influence of different evolutionary forces potentially acting in opposite directions. Such systems provide the opportunity of understanding how potential constraints on morphological variation may influence whole-organism performance. In this study we examined morphology and bite performance in two closely related species of Podarcis wall lizards with divergent microhabitat preferences, to investigate how natural and sexual selection interact to shape the evolution of head traits. Our results show that although head morphology is markedly different between species and sexes, only sexes differ in bite force, indicating that the ecological differentiation between species is reflected in their morphology but does not constrain performance. Rather, the modification of the relative size of head components between species and a shift in the form-function relationship provide a potential explanation of how equal performance is attained by different morphological configurations. Geometric morphometrics provide a clear, biomechanically meaningful image of how this is achieved and show a bisexual pattern of head shape-bite force association in both species. This, together with a strong allometry of head size on body size and head shape on head size, provides indirect morphological evidence for the importance of sexual selection in shaping morphological and functional patterns. Finally, our findings suggest that the differences observed between species and sexes in head traits and bite performance are not reflected in their dietary ecology, implying that if trophic niche segregation between groups occurs, the reasons behind it are not primarily related to head morphology and functional variation.     

Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat‐related patterns within Podarcis bocagei wall lizards

Morphological variation in relation to habitat is known to occur in several lizard groups. Comparative studies have linked morphology and habitat use, showing that locomotion is the principal mediator of this evolutionary relationship. Here, we investigate intraspecific ecomorphological variation in Podarcis bocagei by examining three habitat types, representing a variety between saxicolous and ground‐dwelling habits. Our results indicate variation in absolute and relative limb length, but patterns are only partially concordant to biomechanical predictions. Whereas the femur and hind foot are longer in ground‐dwelling lizards, confirming previous observations, the tibia and hind limb are relatively shorter, contradicting expectations. Additionally, head shape varies substantially between habitats, in line with a hypothesis of mechanical restrictions related to microhabitat and refuge use. Finally, we detect male‐specific variation between habitats in total body size and head size, providing evidence for interactions between natural and sexual selection. Although performance and behaviour studies are necessary to definitely confirm the functional and evolutionary significance of the observed patterns, our study indicates that ecomorphological adaptations can arise in a very short evolutionary time in this group of lizards.     

Variation in the cranium shape of wall lizards (Podarcis spp.): effects of phylogenetic constraints, allometric constraints and ecology

We used geometric morphometrics to explore the influence of phylogenetic and allometric constraints as well as ecology on variation in cranium shape in five species of monophyletic, morphologically similar Podarcis lizards (Podarcis erhardii, Podarcis melisellensis, Podarcis muralis, Podarcis sicula and Podarcis taurica). These species belong to different clades, they differ in their habitat preferences and can be classified into two distinct morphotypes: saxicolous and terrestrial. We found (i) no phylogenetic signal in cranium shape, (ii) diverging allometric slopes among species, and (iii) a significant effect of habitat on cranium shape. The saxicolous species (P. erhardii and P. muralis) had crania with elongated parietals, elongated cranium bases, shortened anterior parts of the dorsal cranium, reduced chambers of the jaw adductor muscles and larger subocular foramina. These cranial features are adaptations that compensate for a flattened cranium, dwelling on vertical surfaces and seeking refuge in crevices. The crania of the terrestrial species (P. melisellensis, P. sicula and P. taurica) tended to be more elongate and robust, with enlarged chambers of the jaw adductor muscle, reduced skull bases and shortened parietals. Terrestrial species exhibited more variation in cranium shape than saxicolous species. Our study suggests that shape variation in Podarcis sp. lizards is largely influenced by ecology, which likely affects species-specific patterns of static allometry.     

Ecomorphological variation in male and female wall lizards and the macroevolution of sexual dimorphism in relation to habitat use

Understanding how phenotypic diversity evolves is a major interest of evolutionary biology. Habitat use is an important factor in the evolution of phenotypic diversity of many animal species. Interestingly, male and female phenotypes have been frequently shown to respond differently to environmental variation. At the macroevolutionary level, this difference between the sexes is frequently analysed using phylogenetic comparative tools to assess variation in sexual dimorphism (SD) across taxa in relation to habitat. A shortcoming of such analyses is that they evaluate the degree of dimorphism itself and therefore they do not provide access to the evolutionary trajectories of each sex. As such, the relative contribution of male and female phenotypes on macroevolutionary patterns of sexual dimorphism cannot be directly assessed. Here, we investigate how habitat use shapes phenotypic diversity in wall lizards using phylogenetic comparative tools to simultaneously assess the tempo and mode of evolution in males, females and the degree of sexual dimorphism. We find that both sexes have globally diversified under similar, but not identical, processes, where habitat use seems to drive macroevolutionary variation in head shape, but not in body size or relative limb length. However, we also observe small differences in the evolutionary dynamics of male and female phenotypes that have a marked impact on macroevolutionary patterns of SD, with important implications for our interpretation of what drives phenotypic diversification within and between the sexes.     

The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini)

Phenotypic differences among species are known to have functional consequences that in turn allow species to use different habitats. However, the role of behaviour in this ecomorphological paradigm is not well defined. We investigated the relationship between morphology, ecology and escape behaviour among 25 species of the lizard clade Liolaemus in a phylogenetic framework. We demonstrate that the relationship between morphology and characteristics of habitat structure shows little or no association, consistent with a previous study on this group. However, a significant relationship was found between morphology and escape behaviour with the distance a lizard moved from a potential predator correlated with body width, axilla-groin length, and pelvis width. A significant relationship between escape behaviour and habitat structure occupation was found; lizards that occupied tree trunks and open ground ran longer distances from predators and were found greater distances from shelter. Behavioural strategies used by these lizards in open habitats appear to have made unnecessary the evolution of limb morphology that has occurred in other lizards from other clades that are found in open settings. Understanding differences in patterns of ecomorphological relationships among clades is an important component for studying adaptive diversification.     

Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis

Recent ecomorphological studies have shown that the predicted correlations between morphology and ecology on broad taxonomic levels are often obscured when comparing more closely related groups. Among species, comparisons of lizards often indicate very little support for adaptive radiations into novel habitats. As few population level studies have been performed, we compared body, head and limb shape between four populations of Urosaurus ornatus living in structurally distinct habitats (cliffs, rocks, trees and boulders). Surprisingly, clear correlations between habitat use and body shape among populations were found, most of which were in good accordance with a priori biomechanical predictions (e.g. flat body and head for extreme climbers; long distal hindlimb segments for jumpers and runners; narrow body and long tail for tree dwelling lizards). This indicates that populations of Urosaurus ornatus are seemingly 'adapted' to the habitat they live in. However, quantification of performance and behaviour are needed to determine the adaptive nature of these observations.     

Burrowing constrains patterns of skull shape evolution in wrasses

The evolution of behavioral and ecological specialization can have marked effects on the tempo and mode of phenotypic evolution. Head-first burrowing has been shown to exert powerful selective pressures on the head and body shapes of many vertebrate and invertebrate taxa. In wrasses, burrowing behaviors have evolved multiple times independently, and are commonly used in foraging and predator avoidance behaviors. While recent studies have examined the kinematics and body shape morphology associated with this behavior, no study to-date has examined the macroevolutionary implications of burrowing on patterns of phenotypic diversification in this clade. Here, we use three-dimensional geometric morphometrics and phylogenetic comparative methods to study the evolution of skull shape in fossorial wrasses and their relatives. We test for skull shape differences between burrowing and non burrowing wrasses and evaluate hypotheses of shape convergence among the burrowing wrasses. We also quantify rates of skull shape evolution between burrowing and non burrowing wrasses to test for whether burrowing constrains or accelerates rates of skull shape evolution in this clade. We find that while burrowing and non burrowing wrasses exhibit similar degrees of morphological disparity, for burrowing wrasses, it took nearly twice as long to amass this disparity. Furthermore, while the disparities between groups are evenly matched, we find that most burrowing species are confined to a particular region of shape space with most species exhibiting narrower heads than many non-burrowing species. These results suggest head-first burrowing constrains patterns of skull shape diversification in wrasses by potentially restricting the range of phenotypes that can perform this behavior.     

Getting in shape: adaptation and phylogenetic inertia in morphology of Australian anuran larvae

The external morphology of frog larvae is predicted to vary among habitats, for a variety of functional reasons. I performed a phylogenetic comparative study to test whether correlations between habitat and the shape of the tadpole and its oral disc are adaptive in 82 species from south‐eastern Australia in the families Hylidae and Myobatrachidae. Habitat distributions and phylogenetic relationships were compiled from the literature and shape was quantified using geometric morphometric analysis of published drawings. Results indicate that shape evolved towards different optima in different habitats while also showing appreciable levels of phylogenetic inertia. Within myobatrachids, evolution of terrestrial tadpoles was associated with a short and shallow head/body and a shallow tail. In aquatic species, the use of benthic microhabitats was correlated with a long shallow tail, dorsal eye position, shallow head/body and ventral mouth with robust jaw sheaths. Even traits with evidence for adaptation evolved slowly in response to habitat shifts, usually requiring ≥10 million years to evolve half‐way to a new optimum. Although these findings support adaptive evolution of tadpole body form, they also highlight a strong influence of ancestral character states and indicate that phenotypes in extant species are partly maladaptive.     

Convergent body flattening in a clade of tropical rock-using lizards (Scincidae: Lygosominae)

The repeated occurrence of similar morphologies in organisms from similar habitats provides good evidence of convergent selection, and convergent patterns of evolutionary change. In lizards, a flattened morphology has often been noted; however, whether this trait is convergent in specific habitats has never been tested using phylogenetic methods. The present study examined patterns of morphological convergence in 18 species of tropical Lygosomine skinks from three broad habitat categories (generalist, leaf litter-dwelling, and rock-using species). In general, although there where relatively few morphological differences of species from different habitats, phylogenetic analyses revealed that rock-using species have consistently and repeatedly evolved a dorsoventrally flattened head and body. The adaptive basis of this flattened morphology is consistent with both biomechanical predictions of performance (e.g. climbing locomotion) and ecology (e.g. use of rock crevices, camouflage) of species that occupy rocky habitats.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 399–411.     

Claw morphometrics in monitor lizards: Variable substrate and habitat use correlate to shape diversity within a predator guild

Numerous studies investigate morphology in the context of habitat, and lizards have received particular attention. Substrate usage is often reflected in the morphology of characters associated with locomotion, and, as a result, claws have become well‐studied ecomorphological traits linking the two. The Kimberley predator guild of Western Australia consists of 10 sympatric varanid species. The purpose of this study was to quantify claw size and shape in the guild using geometric morphometrics, and determine whether these features correlated with substrate use and habitat. Each species was assigned a Habitat/substrate group based on the substrate their claws interact with in their respective habitat. Claw morphometrics were derived for both wild caught and preserved specimens from museum collections, using a 2D semilandmark analysis. Claw shape significantly separated based on Habitat/substrate group. Varanus gouldii and Varanus panoptes claws were associated with sprinting and extensive digging. Varanus mertensi claws were for shallow excavation. The remaining species’ claws reflected specialization for some form of climbing, and differed based on substrate compliance. Varanus glauerti was best adapted for climbing rough sandstone, whereas Varanus scalaris and Varanus tristis had claws ideal for puncturing wood. Phylogenetic signal also significantly influenced claw shape, with Habitat/substrate group limited to certain clades. Positive size allometry allowed for claws to cope with mass increases, and shape allometry reflected a potential size limit on climbing. Claw morphology may facilitate niche separation within this trophic guild, especially when considered with body size. As these varanids are generalist predators, morphological traits associated with locomotion may be more reliable candidates for detecting niche partitioning than those associated directly with diet.     

Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations

The cichlids of East Africa are renowned as one of the most spectacular examples of adaptive radiation. They provide a unique opportunity to investigate the relationships between ecology, morphological diversity, and phylogeny in producing such remarkable diversity. Nevertheless, the parameters of the adaptive radiations of these fish have not been satisfactorily quantified yet. Lake Tanganyika possesses all of the major lineages of East African cichlid fish, so by using geometric morphometrics and comparative analyses of ecology and morphology, in an explicitly phylogenetic context, we quantify the role of ecology in driving adaptive speciation. We used geometric morphometric methods to describe the body shape of over 1000 specimens of East African cichlid fish, with a focus on the Lake Tanganyika species assemblage, which is composed of more than 200 endemic species. The main differences in shape concern the length of the whole body and the relative sizes of the head and caudal peduncle. We investigated the influence of phylogeny on similarity of shape using both distance-based and variance partitioning methods, finding that phylogenetic inertia exerts little influence on overall body shape. Therefore, we quantified the relative effect of major ecological traits on shape using phylogenetic generalized least squares and disparity analyses. These analyses conclude that body shape is most strongly predicted by feeding preferences (i.e., trophic niches) and the water depths at which species occur. Furthermore, the morphological disparity within tribes indicates that even though the morphological diversification associated with explosive speciation has happened in only a few tribes of the Tanganyikan assemblage, the potential to evolve diverse morphologies exists in all tribes. Quantitative data support the existence of extensive parallelism in several independent adaptive radiations in Lake Tanganyika. Notably, Tanganyikan mouthbrooders belonging to the C-lineage and the substrate spawning Lamprologini have evolved a multitude of different shapes from elongated and Lamprologus-like hypothetical ancestors. Together, these data demonstrate strong support for the adaptive character of East African cichlid radiations.     

Categorical versus geometric morphometric approaches to characterizing the evolution of morphological disparity in Osteostraci (Vertebrata,stem Gnathostomata)

Morphological variation (disparity) is almost invariably characterized by two non-mutually exclusive approaches: (1) quantitatively, through geometric morphometrics; and (2) in terms of discrete, ‘cladistic’, or categorical characters. Uncertainty over the comparability of these approaches diminishes the potential to obtain nomothetic insights into the evolution of morphological disparity and the few benchmarking studies conducted so far show contrasting results. Here, we apply both approaches to characterizing morphology in the stem-gnathostome clade Osteostraci in order to assess congruence between these alternative methods as well as to explore the evolutionary patterns of the group in terms of temporal disparity and the influence of phylogenetic relationships and habitat on morphospace occupation. Our results suggest that both approaches yield similar results in morphospace occupation and clustering, but also some differences indicating that these metrics may capture different aspects of morphology. Phylomorphospaces reveal convergence towards a generalized ‘horseshoe’-shaped cranial morphology and two strong trends involving major groups of osteostracans (benneviaspidids and thyestiids), which probably reflect adaptations to different lifestyles. Temporal patterns of disparity obtained from categorical and morphometric approaches appear congruent, however, disparity maxima occur at different times in the evolutionary history of the group. The results of our analyses indicate that categorical and continuous data sets may characterize different patterns of morphological disparity and that discrepancies could reflect preservational limitations of morphometric data and differences in the potential of each data type for characterizing more or less inclusive aspects of overall phenotype.     

Overcoming phylogenetic and geographic uncertainties to test for correlates of range size evolution in gymnophthalmid lizards

Patterns of range size evolution are important for developing an evolutionary biogeographical theory and supporting conservation actions. Determining those patterns is however hampered by multiple factors acting on range size and by our uncertainty with regard to species' phylogenetic relationships and geographic distribution. In addition, given the diversity of analytic approaches existing in the literature, there are concerns regarding whether different methods might lead to different patterns. Here, we addressed these uncertainties in order to test for correlations between the evolution of morphology (body size and shape) and range size. We studied lizards of the family Gymnophthalmidae, representing changes of an order of magnitude in body size and also two independent lineages with limb‐reduced (snake‐like) morphs. We used phylogenetic multivariate methods (pPCA) to control for allometric effects of body size over shape. Then, we performed multiple regressions under three approaches: ‘naive’ least squares, Bayesian comparative methods that accounted for uncertainties in trait optimization, tree topology and branch length, and a novel permutative procedure based on phylogenetic generalized least squares (pGLS) to assess the robustness of our relationships to uncertainties in the range sizes of the species studied. All approaches led to the same answer: only body size was related to range size. While bigger gymnophthalmids tend to have relatively large ranges, small species can have either small or large ones. Our results’ robustness to strong uncertainties in both phylogenetic relationships and range sizes shows there are opportunities for overcoming those problems and produce reliable patterns of range size evolution. However, interpretation of the processes driving patterns of range size evolution will still require advances in phylogenetic and taxonomic knowledge. We discuss the application of morphology–range size relationships to conservation planning in the light of existing uncertainties in the geographic knowledge of our studied species group and workarounds for data availability.