Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity,phylogeny and ecology

Characterizing patterns of observed current variation, and testing hypotheses concerning the potential drivers of this variation, is fundamental to understanding how morphology evolves. Phylogenetic history, size and ecology are all central components driving the evolution of morphological variation, but only recently have methods become available to tease these aspects apart for particular body structures. Extant monitor lizards (Varanus) have radiated into an incredible range of habitats and display the largest body size range of any terrestrial vertebrate genus. Although their body morphology remains remarkably conservative, they have obvious head shape variation. We use two‐dimensional geometric morphometric techniques to characterize the patterns of dorsal head shape variation in 36 species (375 specimens) of varanid, and test how this variation relates to size, phylogenetic history and ecology as represented by habitat. Interspecific head shape disparity is strongly allometric. Once size effects are removed, principal component analysis shows that most shape variation relates to changes in the snout and head width. Size‐corrected head shape variation has strong phylogenetic signal at a broad level, but habitat use is predictive of shape disparity within phylogenetic lineages. Size often explains shape disparity among organisms; however, the ability to separate size and shape variation using geometric morphometrics has enabled the identification of phylogenetic history and habitat as additional key factors contributing to the evolution of head shape disparity among varanid lizards.     

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.     

The role of phylogeny and ecology in shaping morphology in 21 genera and 127 species of Australo‐Papuan myobatrachid frogs

Body shape is predicted to differ among species for functional reasons and in relation to environmental niche and phylogenetic history. We quantified morphological differences in shape and size among 98.5% of the 129 species and all 21 genera of the Australo‐Papuan endemic myobatrachid frogs to test the hypothesis that habitat type predicts body shape in this radiation. We tested this hypothesis in a phylogenetic context at two taxonomic levels: across the entire radiation and within the four largest genera. Thirty‐four external measurements were taken on 623 museum specimens representing 127 species. Data for seven key environmental variables relevant to anurans were assembled for all Australian‐distributed species based on species' distributions and 131,306 locality records. The Australo‐Papuan myobatrachid radiation showed high diversity in adult body size, ranging from minute (15 mm snout–vent length) to very large species (92 mm), and shape, particularly sin relative limb length. Five main morphological and environmental summary variables displayed strong phylogenetic signal. There was no clear relationship between body size and environmental niche, and this result persisted following phylogenetic correction. For most species, there was a better match between environment/habitat and body shape, but this relationship did not persist following phylogenetic correction. At a broad level, species fell into three broad groups based on environmental niche and body shape: 1) species in wet habitats with relatively long limbs, 2) species in arid environments with relatively short limbs (many of which are forward or backward burrowers) and 3) habitat generalist species with a conservative body shape. However, these patterns were not repeated within the four largest genera ? Crinia, Limnodynastes, Pseudophryne and Uperoleia. Each of these genera displayed a highly conservative anuran body shape, yet individual species were distributed across the full spectrum of Australian environments. Our results suggest that phylogenetic legacy is important in the evolution of body size and shape in Australian anurans, but also that the conservative body plan of many frogs works well in a wide variety of habitats.     

Adaptive morphological shifts to novel habitats in marine sculpin fishes

Sculpin fishes of the North American Pacific Coast provide an ideal opportunity to examine whether adaptive morphological character shifts have facilitated occupation of novel habitat types because of their well‐described phylogeny and ecology. In this group, the basal‐rooted species primarily occupy the subtidal habitat, whereas the species in the most distal clades are found in the intertidal. We tested multiple evolutionary models to determine whether changes in body size and changes in number of scales are adaptive for habitat use in sculpins. Based on a statistically robust, highly resolved molecular phylogeny of 26 species of sculpins, in combination with morphometric and habitat affinity data, our analyses show that an adaptive model based on habitat use best explains changes in body size and number of scales. The habitat model was statistically supported over models of neutral evolution, stabilizing selection across all habitats, and three clade‐based models. We suggest that loss of scales and reduction of body size in the intertidal may facilitate cutaneous breathing in air when tidepools become hypoxic during low tides. This study demonstrates how the combined use of phylogenetic, ecological and statistical approaches helps to identify traits that are likely adaptive to novel habitats.     

Habitat transitions alter the adaptive landscape and shape phenotypic evolution in needlefishes (Belonidae)

Habitat occupancy can have a profound influence on macroevolutionary dynamics, and a switch in major habitat type may alter the evolutionary trajectory of a lineage. In this study, we investigate how evolutionary transitions between marine and freshwater habitats affect macroevolutionary adaptive landscapes, using needlefishes (Belonidae) as a model system. We examined the evolution of body shape and size in marine and freshwater needlefishes and tested for phenotypic change in response to transitions between habitats. Using micro‐computed tomographic (µCT) scanning and geometric morphometrics, we quantified body shape, size, and vertebral counts of 31 belonid species. We then examined the pattern and tempo of body shape and size evolution using phylogenetic comparative methods. Our results show that transitions from marine to freshwater habitats have altered the adaptive landscape for needlefishes and expanded morphospace relative to marine taxa. We provide further evidence that freshwater taxa attain reduced sizes either through dwarfism (as inferred from axial skeletal reduction) or through developmental truncation (as inferred from axial skeletal loss). We propose that transitions to freshwater habitats produce morphological novelty in response to novel prey resources and changes in locomotor demands. We find that repeated invasions of different habitats have prompted predictable changes in morphology.     

The contrasted evolutionary fates of deep‐sea chemosynthetic mussels (Bivalvia,Bathymodiolinae)

Bathymodiolinae are giant mussels that were discovered at hydrothermal vents and harboring chemosynthetic symbionts. Due to their close phylogenetic relationship with seep species and tiny mussels from organic substrates, it was hypothesized that they gradually evolved from shallow to deeper environments, and specialized in decaying organic remains, then in seeps, and finally colonized deep‐sea vents. Here, we present a multigene phylogeny that reveals that most of the genera are polyphyletic and/or paraphyletic. The robustness of the phylogeny allows us to revise the genus‐level classification. Organic remains are robustly supported as the ancestral habitat for Bathymodiolinae. However, rather than a single step toward colonization of vents and seeps, recurrent habitat shifts from organic substrates to vents and seeps occurred during evolution, and never the reverse. This new phylogenetic framework challenges the gradualist scenarios “from shallow to deep.” Mussels from organic remains tolerate a large range of ecological conditions and display a spectacular species diversity contrary to vent mussels, although such habitats are yet underexplored compared to vents and seeps. Overall, our data suggest that for deep‐sea mussels, the high specialization to vent habitats provides ecological success in this harsh habitat but also brings the lineage to a kind of evolutionary dead end.     

Morphological divergence between three Arctic charr morphs – the significance of the deep‐water environment

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow‐, deep‐water resource axis in a subarctic postglacial lake (Norway). The two deep‐water (profundal) spawning morphs, a benthivore (PB‐morph) and a piscivore (PP‐morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep‐water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small‐sized PB‐morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep‐water sediments. The PP‐morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO‐morph) predominantly utilizes the shallow benthic–pelagic habitat and food resources. Compared to the deep‐water morphs, the LO‐morph had smaller head relative to body size. The LO‐morph exhibited traits typical for both shallow‐water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep‐water habitat for the PB‐ and PP‐morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep‐water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep‐water piscivore morph has to our knowledge not been described elsewhere.     

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.     

Habitat use affects morphological diversification in dragon lizards

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock‐dwelling, terrestriality, semi‐arboreality and arboreality. Given these reconstructions, we fit models of evolution to species’ morphological trait values and find that rock‐dwelling and arboreality limit diversification relative to terrestriality and semi‐arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model‐averaged rate estimates are slowest for these habitat types. These results suggest that ground‐dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.     

Early burst in body size evolution is uncoupled from species diversification in diving beetles (Dytiscidae)

Changes in morphology are often thought to be linked to changes in species diversification, which is expected to leave a signal of early burst (EB) in phenotypic traits. However, such signal is rarely recovered in empirical phylogenies, even for groups with well‐known adaptive radiation. Using a comprehensive phylogenetic approach in Dytiscidae, which harbours ~4,300 species with as much as 50‐fold variation in body size among them, we ask whether pattern of species diversification correlates with morphological evolution. Additionally, we test whether the large variation in body size is linked to habitat preference and whether the latter influences species turnover. We found, in sharp contrast to most animal groups, that Dytiscidae body size evolution follows an early‐burst model with subsequent high phylogenetic conservatism. However, we found no evidence for associated shifts in species diversification, which point to an uncoupled evolution of morphology and species diversification. We recovered the ancestral habitat of Dytiscidae as lentic (standing water), with many transitions to lotic habitat (running water) that are concomitant to a decrease in body size. Finally, we found no evidence for difference in net diversification rates between habitats nor difference in turnover in lentic and lotic species. This result, together with recent findings in dragonflies, contrasts with some theoretical expectations of the habitat stability hypothesis. Thus, a thorough reassessment of the impact of dispersal, gene flow and range size on the speciation process is needed to fully encompass the evolutionary consequences of the lentic–lotic divide for freshwater fauna.     

The impact of diet,habitat use,and behaviour on head shape evolution in homalopsid snakes

An organism's morphology is driven by selection on function while being constrained by phylogenetic and developmental factors as well as functional trade‐offs. If selection on function is strong and solutions limited, then convergence is expected. In this paper we quantify head shape in a group of ecologically diverse snakes (homalopsid snakes) differing in habitat use and diet using three‐dimensional geometric morphometric approaches. Using data on head shape we explore whether snakes eating different prey show different morphologies. Moreover, we test whether head shape is constrained by other factors such as habitat use, burrow use, or activity pattern. Our results demonstrate similar head shapes in species consuming similar prey. Snakes that capture elusive prey under water differ from those that capture and swallow prey like frogs or crustaceans. Moreover, habitat use, the use of burrows, and activity pattern also significantly impact head shape in this group of snakes. However, this signal appears to be partly confounded by the diet signal. For axes discriminating specifically between habitat use groups or animals that use burrows vs. those that do not shapes were in accordance with our predictions. Our results suggests an adaptive signal in the evolution of head shape in homalopsid snakes with diet, habitat use and the use of burrows all influencing the evolution of head shape in the group.     

Ancient hybridization and phenotypic novelty within Lake Malawi's cichlid fish radiation

Does hybridization play a broad innovative role in evolution? Many studies have shown hybrid origins of individual species, particularly in major adaptive radiations, but this may be a consequence, rather than a cause, of the existence of many closely related species. Cases of hybridization in the early stages of major adaptive radiations are comparatively rare. Here, we report phylogenetic evidence for ancient introgression between distinct lineages of the species-rich Lake Malawi haplochromine cichlid fishes. Mitochondrial DNA (mtDNA) sequences indicated surprisingly close relationships between the shallow-water rocky habitat "Mbuna" species and a group of dark-adapted "Deep-Benthic" species specialized for feeding in low-light conditions (dawn/dusk, under overhangs, and deep water). By contrast, analyses of nuclear amplified fragment length polymorphism data demonstrated that these Deep-Benthic cichlids were more closely related to shallow water "Shallow-Benthic" soft-sediment feeders, a group that shares similar head and body morphology. A coalescent-based computer simulation indicated that the mtDNA similarity of rocky habitat Mbuna species and dark-adapted Deep-Benthic species was due to hybridization rather than incomplete lineage sorting. Comparisons of morphology indicated that some Deep-Benthic species possessed novel morphology not present in other Lake Malawi species groups. Thus, these analyses support the hypothesis that ancient hybridization occurred within the Lake Malawi cichlid radiation, that the event occurred before the radiation of a species group adapted to low-light benthic habitats, and that this group went on to dominate the deep-water regions of Lake Malawi. The results of this study contribute to a growing literature consistent with a creative role of hybridization in the evolution of species diversity and adaptive radiations.     

Spots, stripes, tail tips and dark eyes: Predicting the function of carnivore colour patterns using the comparative method

Animal colour patterns are adaptive for three reasons: camouflage, communication and physico-physiological functions. This study proposes a conceptual framework for predicting the main adaptive function of carnivore colour patterns based on three factors: visibility, shape and location on the body, as well as, their behavioural ecological correlates. Using a comparative phylogenetic approach, the colour patterns present on the body, the tail and the eyes of 200 species of mammalian carnivores were analysed. Their evolutionary history was reconstructed using MacClade and Maddison's concentrated-changes test was used to test the association between species' colour patterns and their behavioural ecology on a composite phylogeny for all the Carnivora. The results for dark spots, vertical stripes, horizontal stripes, ringed tails, black tail tips, white tail tips, dark eye contour and dark eye patches, are presented. The comparative analyses indicate that spotted, vertically striped and horizontally striped coats evolved for camouflage. Tail markings seem to have evolved for intra- and/or inter-specific communication, while dark markings near and around the eyes are associated with variables consistent with a physico-physiological function. These findings suggest that both the physical environment and animal behaviour are important selective factors driving the evolution of animal colour patterns and that both need to be taken into consideration in future studies of animal coloration.     

Phylogeny-Based Comparative Methods Question the Adaptive Nature of Sporophytic Specializations in Mosses

Adaptive evolution has often been proposed to explain correlations between habitats and certain phenotypes. In mosses, a high frequency of species with specialized sporophytic traits in exposed or epiphytic habitats was, already 100 years ago, suggested as due to adaptation. We tested this hypothesis by contrasting phylogenetic and morphological data from two moss families, Neckeraceae and Lembophyllaceae, both of which show parallel shifts to a specialized morphology and to exposed epiphytic or epilithic habitats. Phylogeny-based tests for correlated evolution revealed that evolution of four sporophytic traits is correlated with a habitat shift. For three of them, evolutionary rates of dual character-state changes suggest that habitat shifts appear prior to changes in morphology. This suggests that they could have evolved as adaptations to new habitats. Regarding the fourth correlated trait the specialized morphology had already evolved before the habitat shift. In addition, several other specialized “epiphytic” traits show no correlation with a habitat shift. Besides adaptive diversification, other processes thus also affect the match between phenotype and environment. Several potential factors such as complex genetic and developmental pathways yielding the same phenotypes, differences in strength of selection, or constraints in phenotypic evolution may lead to an inability of phylogeny-based comparative methods to detect potential adaptations.     

A phylogenetic test for adaptive convergence in rock-dwelling lizards

Phenotypic similarity of species occupying similar habitats has long been taken as strong evidence of adaptation, but this approach implicitly assumes that similarity is evolutionarily derived. However, even derived similarities may not represent convergent adaptation if the similarities did not evolve as a result of the same selection pressures; an alternative possibility is that the similar features evolved for different reasons, but subsequently allowed the species to occupy the same habitat, in which case the convergent evolution of the same feature by species occupying similar habitats would be the result of exaptation. Many lizard lineages have evolved to occupy vertical rock surfaces, a habitat that places strong functional and ecological demands on lizards. We examined four clades in which species that use vertical rock surfaces exhibit long hindlimbs and flattened bodies. Morphological change on the phylogenetic branches leading to the rock-dwelling species in the four clades differed from change on other branches of the phylogeny; evolutionary transitions to rock-dwelling generally were associated with increases in limb length and decreases in head depth. Examination of particular characters revealed several different patterns of evolutionary change. Rock-dwelling lizards exhibited similarities in head depth as a result of both adaptation and exaptation. Moreover, even though rock-dwelling species generally had longer limbs than their close relatives, clade-level differences in limb length led to an overall lack of difference between rock- and non-rock-dwelling lizards. These results indicate that evolutionary change in the same direction in independent lineages does not necessarily produce convergence, and that the existence of similar advantageous structures among species independently occupying the same environment may not indicate adaptation.     

Macroecological patterns of sexual size dimorphism in turtles of the world

Sexual size dimorphism (SSD) is a well‐documented phenomenon in both plants and animals; however, the ecological and evolutionary mechanisms that drive and maintain SSD patterns across geographic space at regional and global scales are understudied, especially for reptiles. Our goal was to examine geographic variation of turtle SSD and to explore ecological and environmental correlates using phylogenetic comparative methods. We use published body size data on 135 species from nine turtle families to examine how geographic patterns and the evolution of SSD are influenced by habitat specialization, climate (annual mean temperature and annual precipitation) and climate variability, latitude, or a combination of these predictor variables. We found that geographic variation, magnitude and direction of turtle SSD are best explained by habitat association, annual temperature variance and annual precipitation. Use of semi‐aquatic and terrestrial habitats was associated with male‐biased SSD, whereas use of aquatic habitat was associated with female‐biased SSD. Our results also suggest that greater temperature variability is associated with female‐biased SSD. In contrast, wetter climates are associated with male‐biased SSD compared with arid climates that are associated with female‐biased SSD. We also show support for a global latitudinal trend in SSD, with females being larger than males towards the poles, especially in the families Emydidae and Geoemydidae. Estimates of phylogenetic signal for both SSD and habitat type indicate that closely related species occupy similar habitats and exhibit similar direction and magnitude of SSD. These global patterns of SSD may arise from sex‐specific reproductive behaviour, fecundity and sex‐specific responses to environmental factors that differ among habitats and vary systematically across latitude. Thus, this study adds to our current understanding that while SSD can vary dramatically across and within turtle species under phylogenetic constraints, it may be driven, maintained and exaggerated by habitat type, climate and geographic location.     

Prepared for the future: A strong signal of evolution toward the adult benthic niche during the pelagic stage in Labrid fishes

The morphology of organisms reflects a balance between their evolutionary history, functional demands, and biomechanical constraints imposed by the immediate environment. In many fish species, a marked shift in the selection regime is evident when pelagic larvae, which swim and feed in the open ocean, settle in their adult benthic habitat. This shift is particularly dramatic in coral‐reef fishes, where the adult habitat is immensely complex. However, whether the adult trophic ecotype affects the morphology of early‐life stages is unclear. We measured a suite of 26 functional‐morphological traits in the head and body of larvae from an ontogenetic series of 16 labrid species. Using phylogenetic comparative methods, we reconstructed the location of adaptive peaks of larvae whose adults are associated with different trophic ecotypes. We found that the morphospace occupation in these larvae is largely driven by divergent adaptations to the adult benthic habitats. The disparity between adaptive peaks is achieved early and does not monotonically increase with size. Our findings thus refute the notion that larvae rapidly acquire the trophic‐specific traits during a metamorphic period immediately prior to settlement. This early specialization might be due to the highly complex musculoskeletal system of the head that cannot be rapidly modified.     

Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments

We know little about on how frequently transitions into new habitats occur, especially the colonization of novel environments that are the most likely to instigate adaptive evolution. One of the most extreme ecological transitions has been the shift in habitat associated with the move from water to land by amphibious fish. We provide the first phylogenetic investigation of these transitions for living fish. Thirty‐three families have species reported to be amphibious and these are likely independent evolutionary origins of fish emerging onto land. Phylogenetic reconstructions of closely related taxa within one of these families, the Blenniidae, inferred as many as seven convergences on a highly amphibious lifestyle. Taken together, there appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families. The colonization of novel habitats by other taxa resulting in less dramatic changes in environment should be equally, if not, more frequent in nature, providing an important prerequisite for subsequent adaptive differentiation.     

The relationship between habitat use and body shape in geckos

Geckos are a highly diverse group of lizards, with more than 1,700 species that exhibit a wide range of behaviors, ecologies, and sizes. However, no study has examined links between habitat use and body shape in pad-bearing geckos. We set out to answer a basic question using a data set of pad-bearing geckos (112 species, 103 pad-bearing, 9 padless, 42 genera): Do geckos that occur in different habitats also differ in body shape? Overall, we found that body shape was surprisingly similar among our sample of pad-bearing species, with the exception of the genus Uroplatus, which was clearly distinct from other geckos due to its depressed body and long limbs. However, the padless geckos differed in body shape from the pad-bearing geckos by having longer arms and legs and less rotund bodies. We found that about half of the pad-bearing species primarily inhabit trees, with the other half, divided approximately equally among rocks, the ground, and mixed habitats. We found no significant links between habitat use and body shape, nor any propensity for larger species to occupy different habitats than smaller species. Padless species tend to inhabit rock and ground substrates. Our results indicate that pad-bearing geckos have a relatively uniform body form, which contrasts with to their diversity in color, size, and behavior. Indeed, our data show that the general gecko body shape is suitable for a wide range of habitats, ranging from arboreal to terrestrial. This pattern is a departure from other ecomorphological studies and suggests that geckos may not easily fit into the mold of adaptive radiation, as suggested by prior studies.