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.     

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.     

Neotropical frogs and mating songs: The evolution of advertisement calls in glassfrogs

Anurans emit advertisement calls with the purpose of attracting mates and repelling conspecific competitors. The evolution of call traits is expected to be associated with the evolution of anatomical and behavioural traits due to the physics of call emission and transmission. The evolution of vocalizations might imply trade‐offs with other energetically costly behaviours, such as parental care. Here, we investigated the association between body size, calling site, parental care and call properties (call duration, number of notes, peak frequency, frequency bandwidth and call structure) of the advertisement calls of glassfrogs (Centrolenidae)—a family of Neotropical, leaf‐dwelling anurans—using phylogenetic comparative methods. We also explored the tempo and mode of evolution of these traits and compared them with those of three morphological traits associated with body size, locomotion and feeding. We generated and compiled acoustic data for 72 glassfrog species (46% of total species richness), including representatives of all genera. We found that almost all acoustic traits have significant, but generally modest, phylogenetic signal. Peak frequency of calls is significantly associated with body size, whereas call structure is significantly associated with calling site and paternal care. Thus, the evolution of body size, calling site and paternal care could constrain call evolution. The estimated disparity of acoustic traits was larger than that of morphological traits and the peak in disparity of acoustic traits generally occurred later in the evolution of glassfrogs, indicating a historically recent outset of the acoustic divergence in this clade.     

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.     

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.     

Habitat primary production and the evolution of body size within the hartebeest clade

Local adaptation is a key process in the evolution of biological diversity but relatively few studies have identified the selective forces that drive trait divergence at low taxonomic levels, particularly amongst mammals. Variation in body size across taxa is fundamental as shown by allometric relationships with numerous physiological, morphological and life-history traits. Differences in adult size across cohorts within populations of temperate ungulates are determined by variation in trophic resource availability during growth, suggesting that natural selection might promote the evolution of size divergence across sister taxa through local adaptation to variation in habitat productivity. We tested this hypothesis in the hartebeest ( Alcelaphu s sp.), an antelope lineage including eight extant (or recently extinct) allopatric subspecies that evolved within the last million years and colonized all the African savannahs. We predicted that body size across the subspecies should correlate positively with habitat productivity across taxon ranges. Mean body size of all the hartebeest taxa was quantified using skull length from museum specimens, and climatic variables were used as surrogates of habitat productivity. Body size across subspecies was positively correlated with rainfall, suggesting that variation in habitat primary production may drive morphological evolution between taxa. Focusing at a low taxonomic level has allowed us to identify a critical selective force that may shape divergence in body size, without the confounding effect of variation in trophic niche. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 431–440.     

Body size evolution simultaneously creates and collapses species boundaries in a clade of scincid lizards

Speciation is generally viewed as an irreversible process, although habitat alterations can erase reproductive barriers if divergence between ecologically differentiated species is recent. Reversed speciation might also occur if geographical contact is established between species that have evolved the same reproductive isolating barrier in parallel. Here, we demonstrate a loss of intrinsic reproductive isolation in a clade of scincid lizards as a result of parallel body size evolution, which has allowed for gene flow where large-bodied lineages are in secondary contact. An mtDNA phylogeny confirms the monophyly of the Plestiodon skiltonianus species complex, but rejects that of two size-differentiated ecomorphs. Mate compatibility experiments show that the high degree of body size divergence imposes a strong reproductive barrier between the two morphs; however, the strength of the barrier is greatly diminished between parallel-evolved forms. Since two large-bodied lineages are in geographical contact in the Sierra Nevada Mountains of California, we were also able to test for postzygotic isolation under natural conditions. Analyses of amplified fragment length polymorphisms show that extensive gene exchange is occurring across the contact zone, resulting in an overall pattern consistent with isolation by distance. These results provide evidence of reversed speciation between clades that diverged from a common ancestor more than 12Myr ago.     

Evolution of extreme ontogenetic allometric diversity and heterochrony in pythons,a clade of giant and dwarf snakes

Ontogenetic allometry, how species change with size through their lives, and heterochony, a decoupling between shape, size, and age, are major contributors to biological diversity. However, macroevolutionary allometric and heterochronic trends remain poorly understood because previous studies have focused on small groups of closely related species. Here, we focus on testing hypotheses about the evolution of allometry and how allometry and heterochrony drive morphological diversification at the level of an entire species‐rich and diverse clade. Pythons are a useful system due to their remarkably diverse and well‐adapted phenotypes and extreme size disparity. We collected detailed phenotype data on 40 of the 44 species of python from 1191 specimens. We used a suite of analyses to test for shifts in allometric trajectories that modify morphological diversity. Heterochrony is the main driver of initial divergence within python clades, and shifts in the slopes of allometric trajectories make exploration of novel phenotypes possible later in divergence history. We found that allometric coefficients are highly evolvable and there is an association between ontogenetic allometry and ecology, suggesting that allometry is both labile and adaptive rather than a constraint on possible phenotypes.     

Relationships of diversity,disparity, and their evolutionary rates in squirrels (Sciuridae)

Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per lineage speciation rates, species richness, disparity, and a time‐invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution.     

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.     

Altitude and life‐history shape the evolution of Heliconius wings

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal‐mating clade are smaller than those in the adult‐mating clade. Interestingly, we find that high‐altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high‐altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae)

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.     

Ecological radiation with limited morphological diversification in salamanders

A major goal of evolutionary biology is to explain morphological diversity among species. Many studies suggest that much morphological variation is explained by adaptation to different microhabitats. Here, we test whether morphology and microhabitat use are related in plethodontid salamanders, which contain the majority of salamander species, and have radiated into a striking diversity of microhabitats. We obtained microhabitat data for 189 species that also had both morphometric and phylogenetic data. We then tested for associations between morphology and microhabitat categories using phylogenetic comparative methods. Associations between morphology and ecology in plethodontids are largely confined to a single clade within one subfamily (Bolitoglossinae), whereas variation in morphology across other plethodontids is unrelated to microhabitat categories. These results demonstrate that ecological radiation and morphological evolution can be largely decoupled in a major clade. The results also offer a striking contrast to lizards, which typically show close relationships between morphology and microhabitat.     

Limb and tail lengths in relation to substrate usage in Tropidurus lizards

A close relationship between morphology and habitat is well documented for anoline lizards. To test the generality of this relationship in lizards, snout-vent, tail, and limb lengths of 18 species of Tropidurus (Tropiduridae) were measured and comparisons made between body proportions and substrate usage. Phylogenetic analysis of covariance by computer simulation suggests that the three species inhabiting sandy soils have relatively longer feet than do other species. Phylogenetic ANCOVA also demonstrates that the three species inhabiting tree canopies and locomoting on small branches have short tails and hind limbs. These three species constitute a single subclade within the overall Tropidurus phylogeny and analyses with independent contrasts indicate that divergence in relative tail and hind limb length has been rapid since they split from their sister clade. Being restricted to a single subclade, the difference in body proportions could logically be interpreted as either an adaptation to the clade's lifestyle or simply a nonadaptive synapomorphy for this lineage. Nevertheless, previous comparative studies of another clade of lizards (Anolis) as well as experimental studies of Sceloporus lizards sprinting on rods of different diameters support the adaptive interpretation.     

Does ‘gliding while gravid’ explain Rensch's rule in flying lizards?

Among species with sexual size dimorphism (SSD), taxa in which males are the larger sex have increasing SSD with increasing body size, whereas in taxa in which females are the larger sex, SSD decreases with body size: Rensch's rule. We show in flying lizards, a clade of mostly female‐larger species, that SSD increases with body size, a pattern similar to that in clades with male‐biased SSD or more evenly mixed SSD. The observed pattern in Draco appears due to SSD increasing with evolutionary changes in male body size; specifically divergence in body size among species that are in sympatric congeneric assemblages. We suggest that increasing body size, resulting in decreased gliding performance, reduces the relative gliding cost of gravidity in females, and switches sexual selection in males away from a small‐male, gliding advantage and toward selection on large size and fighting ability as seen in many other lizards. Thus, selection for large females is likely greater than selection for large males at the smaller end of the body size continuum, whereas this relationship reverses for species at the larger end of the continuum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 270–282.     

Body mass explains characteristic scales of habitat selection in terrestrial mammals

Niche theory in its various forms is based on those environmental factors that permit species persistence, but less work has focused on defining the extent, or size, of a species' environment: the area that explains a species' presence at a point in space. We proposed that this habitat extent is identifiable from a characteristic scale of habitat selection, the spatial scale at which habitat best explains species' occurrence. We hypothesized that this scale is predicted by body size. We tested this hypothesis on 12 sympatric terrestrial mammal species in the Canadian Rocky Mountains. For each species, habitat models varied across the 20 spatial scales tested. For six species, we found a characteristic scale; this scale was explained by species' body mass in a quadratic relationship. Habitat measured at large scales best-predicted habitat selection in both large and small species, and small scales predict habitat extent in medium-sized species. The relationship between body size and habitat selection scale implies evolutionary adaptation to landscape heterogeneity as the driver of scale-dependent habitat selection.     

Sexual selection is positively associated with ecological generalism among agamid lizards

Natural and sexual selection shape the evolution of species but the interplay between them is poorly understood. Two phylogenetic studies on birds have suggested that species with greater sexual dichromatism have a broader habitat use. We show that in agamid lizards, species with more elaborate secondary sexual traits are also ecologically more opportunistic. Species with greater dimorphism in head size and ornamentation have greater altitudinal range and broader habitat use, respectively, and species with greater sexual dichromatism have wider microhabitat use. Body size was positively associated with sexual and ecological generalism, but associations between ecological and sexual traits remained after accounting for body size. We suggest that sexual and natural selection may be linked either because sexual selection can promote generalism at the population level by favouring 'good genes', or because higher population densities may be associated with both stronger sexual selection and broader resource use.     

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.