Morphological evolution of the lizard skull: a geometric morphometrics survey

Patterns of diversity among lizard skulls were studied from a morphological, phylogenetic, and functional perspective. A sample of 1,030 lizard skulls from 441 species in 17 families was used to create a lizard skull morphospace. This morphospace was combined with a phylogeny of lizard families to summarize general trends in the evolution of the lizard skull. A basal morphological split between the Iguania and Scleroglossa was observed. Iguanians are characterized by a short, high skull, with large areas of attachment for the external adductor musculature, relative to their sister group. The families of the Iguania appear to possess more intrafamilial morphological diversity than families of the Scleroglossa, but rarefaction of the data reveals this to be an artifact caused by the greater number of species represented in Iguanian families. Iguanian families also appear more dissimilar to one another than families of the Scleroglossa. Permutation tests indicate that this pattern is real and not due to the smaller number of families in the Iguanidae. Parallel and convergent evolution is observed among lizards with similar diets: ant and termite specialists, carnivores, and herbivores. However, these patterns are superimposed over the more general phylogenetic pattern of lizard skull diversity. This study has three central conclusions. Different clades of lizards show different patterns of disparity and divergence in patterns of morphospace occupation. Phylogeny imposes a primary signal upon which a secondary ecological signal is imprinted. Evolutionary patterns in skull metrics, taken with functional landmarks, allow testing of trends and the development of new hypotheses concerning both shape and biomechanics.     

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.     

RHYTIDOSTEID TEMNOSPONDYLS IN GONDWANA: A NEW TAXON FROM THE LOWER TRIASSIC OF BRAZIL

Abstract:  A new South American Early Triassic stereospondyl is described and considered to represent a new taxon, Cabralia lavinai gen. et sp. nov. The material consists of two well-preserved skull fragments. According to recent phylogenetic analyses of rhytidosteids and related taxa, the new taxon is referred to the Rhytidosteidae based on the presence of orbits that are located close to the skull margins, an otic notch that is reduced to an embayment, tabular horns that are reduced and broad based, a straight posterior margin of the palate, skull sculpture with nodules and pustules, and a 'twisted' quadrate ramus of the pterygoid. The presence of a prominent lacrimal bone suggests a basal position within Rhytidosteidae for C. lavinai , and possibly a close relationship with the Indian Indobrachyops , because all other known rhytidosteids exhibit the derived condition of an absence of the lacrimal. The presence of a basal rhytidosteid in the Paraná Basin of South America strongly supports previous hypotheses of a Gondwanan origin and radiation of stereospondyl temnospondyls during the Early Triassic, but leaves unresolved the question of where exactly they arose within that region.     

Origins,bottlenecks, and present‐day diversity: Patterns of morphospace occupation in marine bivalves

It has long been known that species should not be distributed randomly in morphospace (a multidimensional trait space), even under simple models of evolution. However, recent studies suggest that position in morphospace can affect aspects of evolution such as the durations of clades and the species richness of their constituent taxa. Here we investigate the dynamics of morphospace occupancy in living and fossil marine bivalves using shell size and aspect ratio, two functionally important traits. Multiple lines of evidence indicate that the center of a family's morphospace today represents a location where taxonomic diversity is maximized, apparently owing to lower extinction rates. Within individual bivalve families, species with narrow geographic ranges are distributed throughout the morphospace but widespread species, which are generally expected to be extinction resistant, tend to be concentrated near the center. The morphospace centers of most species‐rich families today (defined as the median value for all species in the family) tend to be close to the positions of the family founders, further suggesting an association between position in morphospace and net diversification rates. However, trajectories of individual subclades (genera) are inconsistent with the center of morphospace being an evolutionary attractor.     

Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach

Understanding how and why certain clades diversify greatly in morphology whereas others do not remains a major theme in evolutionary biology. Projecting families of phylogenies into multivariate morphospaces can distinguish two scenarios potentially leading to unequal morphological diversification: unequal magnitude of change per phylogenetic branch, and unequal efficiency in morphological innovation. This approach is demonstrated using a case study of skulls in sister clades within the South American fish superfamily Anostomoidea. Unequal morphological diversification in this system resulted not from the morphologically diverse clade changing more on each phylogenetic branch, but from that clade distributing an equal amount of change more widely through morphospace and innovating continually. Although substantial morphological evolution occurred throughout the less diverse clade's history, most of that clade's expansion in morphospace occurred in the most basal branches, and more derived portions of that radiation oscillated within previously explored limits. Because simulations revealed that there is a maximum 2.7% probability of generating two clades that differ so greatly in the density of lineages within morphospace under a null Brownian model, the observed difference in pattern likely reflects a difference in the underlying evolutionary process. Clade-specific factors that may have promoted or arrested morphological diversification are discussed.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

PARALLEL RACE FORMATION AND THE EVOLUTION OF MIMICRY IN HELICONIUS BUTTERFLIES: A PHYLOGENETIC HYPOTHESIS FROM MITOCHONDRIAL DNA SEQUENCES

Mimicry has been a fundamental focus of research since the birth of evolutionary biology yet rarely has been studied from a phylogenetic perspective beyond the simple recognition that mimics are not similar due to common descent. The difficulty of finding characters to discern relationships among closely related and convergent taxa has challenged systematists for more than a century. The phenotypic diversity of wing pattens among mimetic Heliconius adds an additional twist to the problem, because single species contain more than a dozen radically different-looking geographical races even though the mimetic advantage is theoretically highest when all individuals within and between species appear the same. Mitochondrial DNA (mtDNA) offers an independent way to address these issues. In this study, Cytochrome Oxidase I and II sequences from multiple, parallel races of Heliconius erato and Heliconius melpomene are examined, to estimate intraspecific phylogeny and gauge sequence divergence and ages of clades among races within each species. Although phenotypes of sympatric races exhibit remarkable concordance between the two species, the mitochondrial cladograms show that the species have not shared a common evolutionary history. H. erato exhibits a basal split between trans- and cis-Andean groups of races, whereas H. melpomene originates in the Guiana Shield. Diverse races in either species appear to have evolved within the last 200,000 yr, and convergent phenotypes have evolved independently within as well as between species. These results contradict prior theories of the evolution of mimicry based on analysis of wing-pattern genetics.     

A phylogenetic view on skull size and shape variation in the smooth newt (Lissotriton vulgaris,Caudata, Salamandridae)

In this study, we explore skull size and shape variation in the smooth newt, a taxon with substantial morphological differentiation and complex phylogeographic relations. By projecting phylogenies into the morphospace of the skull shape, we explore the variation in and differentiation of this complex morphological structure within a phylogenetic framework. For these analyses, we used a dataset that covers the most southern part of the species’ distribution range, including all conventionally recognized subspecies. The study revealed different patterns of divergence in skull shape between sexes, which is paralleled by intraspecific differentiation. The divergence in dorsal skull shape is concordant with the phylogenetic divergence, as the most diverged clades of the smooth newt (Lissotriton vulgaris kosswigi and Lissotriton vulgaris lantzi) exhibit a skull shape that significantly diverges from the smooth newt’s mean shape configuration. The results of this study also indicate that ventral skull portion, which is more directly related to feeding and foraging, shows higher variation between populations than dorsal skull portion, which appears to be less variable and phylogenetically informative.     

The evolution of morphological diversity in continental assemblages of passerine birds

Understanding geographic variation in the species richness and lineage composition of regional biotas is a long‐standing goal in ecology. Why do some evolutionary lineages proliferate while others do not, and how do new colonists fit into an established fauna? Here, we analyze the morphological structure of assemblages of passerine birds in four biogeographic regions to examine the relative influence of colonization history and niche‐based processes on continental communities of passerine birds. Using morphological traits related to habitat choice, foraging technique, and movement, we quantify the morphological spaces occupied by different groups of passerine birds. We further quantify morphological overlap between groups by multivariate discriminant analysis and null model analyses of trait dispersion. Finally, we use subclade disparity through time to assess the temporal component of morphological evolution. We find mixed support for the prediction, based on priority, that first colonizers constrain subsequent colonizers. Indeed, our results show that the assembly of continental communities is idiosyncratic with regards to the diversification of new clades and the filling of morphospace.     

Convergence and divergence in the evolution of cat skulls: temporal and spatial patterns of morphological diversity

Background

Studies of biological shape evolution are greatly enhanced when framed in a phylogenetic perspective. Inclusion of fossils amplifies the scope of macroevolutionary research, offers a deep-time perspective on tempo and mode of radiations, and elucidates life-trait changes. We explore the evolution of skull shape in felids (cats) through morphometric analyses of linear variables, phylogenetic comparative methods, and a new cladistic study of saber-toothed cats.

Methodology/Principal Findings

A new phylogenetic analysis supports the monophyly of saber-toothed cats (Machairodontinae) exclusive of Felinae and some basal felids, but does not support the monophyly of various saber-toothed tribes and genera. We quantified skull shape variation in 34 extant and 18 extinct species using size-adjusted linear variables. These distinguish taxonomic group membership with high accuracy. Patterns of morphospace occupation are consistent with previous analyses, for example, in showing a size gradient along the primary axis of shape variation and a separation between large and small-medium cats. By combining the new phylogeny with a molecular tree of extant Felinae, we built a chronophylomorphospace (a phylogeny superimposed onto a two-dimensional morphospace through time). The evolutionary history of cats was characterized by two major episodes of morphological divergence, one marking the separation between saber-toothed and modern cats, the other marking the split between large and small-medium cats.

Conclusions/Significance

Ancestors of large cats in the ‘Panthera’ lineage tend to occupy, at a much later stage, morphospace regions previously occupied by saber-toothed cats. The latter radiated out into new morphospace regions peripheral to those of extant large cats. The separation between large and small-medium cats was marked by considerable morphologically divergent trajectories early in feline evolution. A chronophylomorphospace has wider applications in reconstructing temporal transitions across two-dimensional trait spaces, can be used in ecophenotypical and functional diversity studies, and may reveal novel patterns of morphospace occupation.     

Flightlessness affects cranial morphology in birds

Flightless birds belonging to phylogenetically distant clades share several morphological features in the pectoral and pelvic apparatus. There are indications that skull morphology is also influenced by flightlessness. In this study we used a large number of flightless species to test whether flightlessness in modern birds does indeed affect cranial morphology. Discriminant analyses and variation partitioning show evidence for a relationship between skull morphology and the flightless condition in birds. A possible explanation for the change in cranial morphology can be linked to the reduced selective force for light-weight skulls in flightless birds. This makes an increase in muscle mass, and therefore an enlargement of muscle insertion areas on the skull, possible. We also compared the ontogenetic trajectory of Gallus with the adult morphology of a sample of flightless species to see whether the apomorphic features characterizing the skull of flightless birds share the same developmental basis, which would indicate convergent evolution by parallelism. Skull morphology (expressed as principal component scores) of palaeognathous flightless birds (ratites) is dissimilar (higher scores) to juvenile stages of the chicken and therefore seem peramorphic (overdeveloped). Principal component scores of adult neognathous flightless birds fall within the range of chicken development, so no clear conclusions about the ontogenetic trajectories leading to their sturdier skull morphology could be drawn.     

Evolution of skull and mandible shape in cats (Carnivora: Felidae)

The felid family consists of two major subgroups, the sabretoothed and the feline cats, to which all extant species belong, and are the most anatomically derived of all carnivores for predation on large prey with a precision killing bite. There has been much controversy and uncertainty about why the skulls and mandibles of sabretoothed and feline cats evolved to become so anatomically divergent, but previous models have focused on single characters and no unifying hypothesis of evolutionary shape changes has been formulated. Here I show that the shape of the skull and mandible in derived sabrecats occupy entirely different positions within overall morphospace from feline cats, and that the evolution of skull and mandible shape has followed very different paths in the two subgroups. When normalised for body-size differences, evolution of bite forces differ markedly in the two groups, and are much lower in derived sabrecats, and they show a significant relationship with size and cranial shape, whereas no such relationship is present in feline cats. Evolution of skull and mandible shape in modern cats has been governed by the need for uniform powerful biting irrespective of body size, whereas in sabrecats, shape evolution was governed by selective pressures for efficient predation with hypertrophied upper canines at high gape angles, and bite forces were secondary and became progressively weaker during sabrecat evolution. The current study emphasises combinations of new techniques for morphological shape analysis and biomechanical studies to formulate evolutionary hypotheses for difficult groups.     

DISPARITY: MORPHOLOGICAL PATTERN AND DEVELOPMENTAL CONTEXT

Abstract:  The distribution of organic forms is clumpy at any scale from populations to the highest taxonomic categories, and whether considered within clades or within ecosystems. The fossil record provides little support for expectations that the morphological gaps between species or groups of species have increased through time as it might if the gaps were created by extinction of a more homogeneous distribution of morphologies. As the quantitative assessments of morphology have replaced counts of higher taxa as a metric of morphological disparity, numerous studies have demonstrated the rapid construction of morphospace early in evolutionary radiations, and have emphasized the difference between taxonomic measures of morphological diversity and quantitative assessments of disparity. Other studies have evaluated changing patterns of disparity across mass extinctions, ecomorphological patterns and the patterns of convergence within ecological communities, while the development of theoretical morphology has greatly aided efforts to understand why some forms do not occur. A parallel, and until recently, largely separate research effort in evolutionary developmental biology has established that the developmental toolkit underlying the remarkable breadth of metazoan form is largely identical among Bilateria, and many components are shared among all metazoa. Underlying this concern with disparity is a question about temporal variation in the production of morphological innovations, a debate over the relative significance of the generation of new morphologies vs. differential probabilities of their successful introduction, and the relative importance of constraint, convergence and contingency in the evolution of form.     

Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents

It has been hypothesized that most morphological evolution occurs by allometric differentiation. Because rodents encapsulate a phenomenal amount of taxonomic diversity and, among several clades, contrasting levels of morphological diversity, they represent an excellent subject to address the question: how variable are allometric patterns during evolution? We investigated the influence of phylogenetic relations and ecological factors on the results of the first quantification of allometric disparity among rodents by exploring allometric space, a multivariate morphospace here derived from, and encapsulating all, the ontogenetic trajectories of 34 rodent species from two parallel phylogenetic radiations. Disparity was quantified using angles between ontogenetic trajectories for different species and clades. We found an overlapping occupation of allometric space by muroid and hystricognath species, revealing both clades possess similar abilities to evolve in different directions of phenotypic space, and anatomical diversity does not act to constrain the labile nature of allometric patterning. Morphological features to enable efficient processing of food serve to group rodents in allometric space, reflecting the importance of convergent morphology, rather than shared evolutionary history, in the generation of allometric patterns. Our results indicate that the conserved level of morphological integration found among primates cannot simply be extended to all mammals.     

The skull evolution of oviraptorosaurian dinosaurs: the role of niche partitioning in diversification

Oviraptorosaurs are bird‐like theropod dinosaurs that thrived in the final pre‐extinction ecosystems during the latest Cretaceous, and the beaked, toothless skulls of derived species are regarded as some of the most peculiar among dinosaurs. Their aberrant morphologies are hypothesized to have been caused by rapid evolution triggered by an ecological/biological driver, but little is known about how their skull shapes and functional abilities diversified. Here, we use quantitative techniques to study oviraptorosaur skull form and mandibular function. We demonstrate that the snout is particularly variable, that mandibular form and upper/lower beak form are significantly correlated with phylogeny, and that there is a strong and significant correlation between mandibular function and mandible/lower beak shape, suggesting a form–function association. The form–function relationship and phylogenetic signals, along with a moderate allometric signal in lower beak form, indicate that similar mechanisms governed beak shape in oviraptorosaurs and extant birds. The two derived oviraptorosaur clades, oviraptorids and caenagnathids, are significantly separated in morphospace and functional space, indicating that they partitioned niches. Oviraptorids coexisting in the same ecosystem are also widely spread in morphological and functional space, suggesting that they finely partitioned feeding niches, whereas caenagnathids exhibit extreme disparity in beak size. The diversity of skull form and function was likely key to the diversification and evolutionary success of oviraptorosaurs in the latest Cretaceous.     

Do key innovations unlock diversification? A case-study on the morphological and ecological impact of pharyngognathy in acanthomorph fishes

Key innovations may allow lineages access to new resources and facilitate the invasion of new adaptive zones, potentially influencing diversification patterns. Many studies have focused on the impact of key innovations on speciation rates, but far less is known about how they influence phenotypic rates and patterns of ecomorphological diversification. We use the repeated evolution of pharyngognathy within acanthomorph fishes, a commonly cited key innovation, as a case study to explore the predictions of key innovation theory. Specifically, we investigate whether transitions to pharyngognathy led to shifts in the rate of phenotypic evolution, as well as shifts and/or expansion in the occupation of morphological and dietary space, using a dataset of 8 morphological traits measured across 3,853 species of Acanthomorpha. Analyzing the 6 evolutionarily independent pharyngognathous clades together, we found no evidence to support pharyngognathy as a key innovation; however, comparisons between individual pharyngognathous lineages and their sister clades did reveal some consistent patterns. In morphospace, most pharyngognathous clades cluster in areas that correspond to deeper-bodied morphologies relative to their sister clades, while occupying greater areas in dietary space that reflects a more diversified diet. Additionally, both Cichlidae and Labridae exhibited higher univariate rates of phenotypic evolution compared with their closest relatives. However, few of these results were exceptional relative to our null models. Our results suggest that transitions to pharyngognathy may only be advantageous when combined with additional ecological or intrinsic factors, illustrating the importance of accounting for lineage-specific effects when testing key innovation hypotheses. Moreover, the challenges we experienced formulating informative comparisons, despite the ideal evolutionary scenario of multiple independent evolutionary origins of pharyngognathous clades, illustrates the complexities involved in quantifying the impact of key innovations. Given the issues of lineage specific effects and rate heterogeneity at macroevolutionary scales we observed, we suggest a reassessment of the expected impacts of key innovations may be warranted.     

The ontogenetic complexity of developmental constraints

Developmental constraint is a theoretically important construct bridging ontogenetic and evolutionary studies. We propose a new operationalization of this notion that exploits the unusually rich measurement structure of landmark data. We represent landmark configurations by their partial warps, a basis for morphospace that represents a set of localized features of form. A finding of developmental constraint arises from the interplay between age-varying means and age-specific variances in these subspaces of morphospace. Examination of variances and means in 16 ventral skull landmarks in the cotton rat S. fulviventer at ages 1, 10, 20, and 30 days yielded three types of developmental constraint: canalization (constraint to relatively constant form age by age); chreods (reduction of variance orthogonal to the mean trajectory over ages); and opposition (reduction of age-specific variance along the mean trajectory over ages). While canalization and chreodic constraints have been noted previously, the oppositional type of constraint appears novel. Only one of our characters, relative length and orientation of the incisive foramen, appears to be canalized. Although skull growth becomes increasingly integrated through ontogeny, our characters display a remarkable spatiotemporal complexity in patterns of variance reduction. The specific assortment of constraints observed may be related to the precociality of Sigmodon. We suggest that Waddington's diagrammatic presentation of the “epigenetic landscape” may be misleading in quantitative studies of developmental regulation.     

Cats and Dogs Down the Tree: The Tempo and Mode of Evolution in the Lower Carnassial of Fossil and Living Carnivora

Teeth are usually considered the primer to understand mammalian evolution. Their morphology is the result of the complex interplay between adaptation to food processing and somewhat fixed developmental programs. We analyse the morphometry of the first lower molar (m1 = lower carnassial) in 199 carnivore species (64 extant and 135 extinct) in order to clarify the tempo and mode of evolution of two different and possibly related traits, tooth size and tooth angular height. We applied a set of comparative methods and produced disparity through time plots by using four alternative phylogenetic trees. Three of them include fossil species, and were used in order to estimate what an effect the inclusion of fossil species has on the patterns we found for extant species. Our analyses on living species show that m1 size exhibits a weak phylogenetic signal, and that its variance occurs more within than among clades. The opposite applies to m1 angular height, which evolved in an adaptive radiation-like fashion, showing very strong phylogenetic signal and great among-clade variation. These results are thoroughly confirmed after the inclusion of fossil data. Major differences in m1 shape in Carnivora were clearly established early in their evolutionary history, probably as a result of rapid morphospace occupation after the clade radiation. Successive variation in tooth size allowed species to avoid potential overlap in feeding morphologies as a mechanism to limit interspecific competitive interaction within subclades.     

Why are There Fewer Marsupials than Placentals? On the Relevance of Geography and Physiology to Evolutionary Patterns of Mammalian Diversity and Disparity

Placental mammals occupy a larger morphospace and are taxonomically more diverse than marsupials by an order of magnitude, as shown by quantitative and phylogenetic studies of several character complexes and clades. Many have suggested that life history acts as a constraint on the evolution of marsupial morphology. However, the frequent circumvention of constraints suggests that the pattern of morphospace occupation in marsupials is more a reflection of lack of ecological opportunity than one of biases in the production of variants during development. Features of marsupial physiology are a potential source of biases in the evolution of the group; these could be coupled with past macroevolutionary patterns that followed conditions imposed by global temperature changes. This is evident at the K/Pg boundary and at the Eocene/Oligocene boundary. The geographic pattern of taxonomic and morphological diversity in placental clades mirrors that of extant placentals as a whole versus marsupials: placentals of northern origin are more diverse those of southern one and include the clades that are outliers in taxonomic (rodents and bats) and ecomorphological (whales and bats) richness.