Phylogenetic implications of the morphology of the braincase of caecilian amphibians (Gymnophiona)

Caecilian morphology is strongly modified in association with their fossorial mode of life. Currently phylogenetic analyses of characters drawn from the morphology of caecilians lack resolution, as well as complementarity, with results of phylogenetic analyses that employ molecular data. Stemming from the hypothesis derived from the mammal literature that the braincase has the greatest potential (in comparison to other cranial units) to yield phylogenetic information, the braincase and intimately associated stapes of 27 species (23 genera) of extant caecilians were examined using images assembled via microcomputed tomography. Thirty‐four new morphological characters pertaining to the braincase and stapes were identified and tested for congruence with previously recognized morphological characters. The results reveal that when added to previous character matrices, characters of the braincase and stapes resolve generic‐level relationships in a way that is largely congruent with the results of molecular analyses. Analysis of a combined data set of molecular and morphological data provides a framework for conducting ancestral character state reconstructions, which resulted in the identification of 95 new synapomorphies for various clades and taxa, 27 of which appear to be unique for the taxa that possess them. Together these data demonstrate the utility of the application of characters of the braincase and stapes for resolving phylogenetic relationships for a group whose morphology is largely confounded by functional modifications. In addition this study provides evidence of the utility of the braincase in resolving problematic morphology‐based phylogeny outside of Amniota, in an amphibian group. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166 , 160–201.     

The role of character loss in phylogenetic reconstruction as exemplified for the Annelida

Annelid relationships are controversial, and molecular and morphological analyses provide incongruent estimates. Character loss is identified as a major confounding factor for phylogenetic analyses based on morphological data. A direct approach and an indirect approach for the identification of character loss are discussed. Character loss can frequently be found within annelids and examples of the loss of typical annelid characters, like chaetae, nuchal organs, coelomic cavities and other features, are given. A loss of segmentation is suggested for Sipuncula and Echiura; both are supported as annelid ingroups in molecular phylogenetic analyses. Moreover, character loss can be caused by some modes of heterochronic evolution (paedomorphosis) and, as shown for orbiniid and arenicolid polychaetes, paedomorphic taxa might be misplaced in phylogenies derived from morphology. Different approaches for dealing with character loss in cladistic analyses are discussed. Application of asymmetrical character state transformation costs or usage of a dynamic homology framework represents promising approaches. Identifying character loss prior to a phylogenetic analysis will help to refine morphological data matrices and improve phylogenetic analyses of annelid relationships.     

Morphology and angiosperm systematics in the molecular era

Several ways in which morphology is used in systematic and evolutionary research in angiosperms are shown and illustrated with examples: 1) searches for special structural similarities, which can be used to find hints for hitherto unrecognized relationships in groups with unresolved phylogenetic position; 2) cladistic studies based on morphology and combined morphological and molecular analyses; 3) comparative morphological studies in new, morphologically puzzling clades derived from molecular studies; 4) studies of morphological character evolution, unusual evolutionary directions, and evolutionary lability based on molecular studies; and 5) studies of organ evolution. Conclusions: Goals of comparative morphology have shifted in the present molecular era. Morphology no longer plays the primary role in phylogenetic studies. However, new opportunities for morphology are opening up that were not present in the premolecular era: 1) phylogenetic studies with combined molecular and morphological analyses; 2) reconstruction of the evolution of morphological features based on molecularly derived cladograms; 3) refined analysis of morphological features induced by inconsistencies of previous molecular and molecular phylogenetic analyses; 4) better understanding of morphological features by judgment in a wider biological context; 5) increased potential for including fossils in morphological analyses; and 6) exploration of the evolution of morphological traits by integration of comparative structural and molecular developmental genetic aspects (Evo-Devo); this field is still in its infancy in botany; its advancement is one of the major goals of evolutionary botany.     

An Expanded Combined Evidence Approach to the Gavialis Problem Using Geometric Morphometric Data from Crocodylian Braincases and Eustachian Systems

The phylogenetic position of the Indian gharial (Gavialis gangeticus) is disputed - morphological characters place Gavialis as the sister to all other extant crocodylians, whereas molecular and combined analyses find Gavialis and the false gharial (Tomistoma schlegelii) to be sister taxa. Geometric morphometric techniques have only begun to be applied to this issue, but most of these studies have focused on the exterior of the skull. The braincase has provided useful phylogenetic information for basal crurotarsans, but has not been explored for the crown group. The Eustachian system is thought to vary phylogenetically in Crocodylia, but has not been analytically tested. To determine if gross morphology of the crocodylian braincase proves informative to the relationships of Gavialis and Tomistoma, we used two- and three-dimensional geometric morphometric approaches. Internal braincase images were obtained using high-resolution computerized tomography scans. A principal components analysis identified that the first component axis was primarily associated with size and did not show groupings that divide the specimens by phylogenetic affinity. Sliding semi-landmarks and a relative warp analysis indicate that a unique Eustachian morphology separates Gavialis from other extant members of Crocodylia. Ontogenetic expansion of the braincase results in a more dorsoventrally elongate median Eustachian canal. Changes in the shape of the Eustachian system do provide phylogenetic distinctions between major crocodylian clades. Each morphometric dataset, consisting of continuous morphological characters, was added independently to a combined cladistic analysis of discrete morphological and molecular characters. The braincase data alone produced a clade that included crocodylids and Gavialis, whereas the Eustachian data resulted in Gavialis being considered a basally divergent lineage. When each morphometric dataset was used in a combined analysis with discrete morphological and molecular characters, it generated a tree that matched the topology of the molecular phylogeny of Crocodylia.     

Morphology and phylogenetic significance of the pectoral articular region in elasmobranchs (Chondrichthyes)

The morphology of the articular region of the scapulocoracoid and the basal cartilages of the pectoral fin endoskeleton of elasmobranchs is reviewed in detail. Examination of this specific morphology in more than 140 species of elasmobranchs (of which 40 are reported here) revealed characters that may have a bearing on the higher‐level phylogeny of the group. Ten distinct characters of the scapular articular region of elasmobranchs are described, varying in terms of the number of distinct articular sites as well as their specific morphology (e.g. whether the articular surface is composed of condyles and/or facets). Previous interpretations of the articular region in morphological phylogenies are also reviewed, revealing much more morphological variation than formerly reported. These prior characters played an important role in supporting the Hypnosqualea, and may still be derived for this clade. The variation and distribution of the new characters discussed provide new insights for the evolution of the pectoral endoskeleton in chondrichthyans. They also highlight the continued importance of morphological characters for phylogenetic studies, and reinforce the necessity of in‐depth anatomical reviews of certain characters employed in previous higher‐level phylogenetic studies of elasmobranchs. © 2015 The Linnean Society of London     

Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda)

Organismic diversity, as well as distributional and ecological patterns, can be fully understood in an evolutionary framework only. Reliable phylogenetic trees are required to ‘read history’, but are not yet available for most marine invertebrate groups. Molecular systematics offers an enormous potential, but still fails for ‘all‐species approaches’ on groups with species that are rare or occur in remote areas only, simply because there is no easily collectable material available for sequence analyses. Exploring morphologically aberrant corambid nudibranch gastropods as a case study, we assess whether or not morphology‐based phylogenetic analyses can fill this gap and produce a tree that allows a detailed view on evolutionary history. Morphology‐based parsimony analysis of corambids and potential relatives resulted in a well‐resolved and remarkably robust topology. As an offshoot of kelp‐associated onchidoridid ancestors, and obviously driven by the heterochronic shortening of life cycles and morphological juvenilization in an ephemeral habitat, the ancestor of corambids originated in cool northern Pacific coastal waters. A basal clade (the genus Loy) diverged there, adapting to live on soft bottoms under successive reversals of paedomorphic traits. The more speciose Corambe lineage radiated preying upon short‐lived encrusting bryozoa in a high‐energy kelp environment. Selection favoured transformation of the mantle into a cuticle‐covered shield, and successive paedomorphic translocations of dorid anal gills to the protected ventral side of the body, where compensatory, multiple gills evolved. Corambe species probably first colonized tropical American seas, and then radiated in worldwide temperate waters: this is explained by the excellent long‐distance dispersal abilities afforded by rafting on kelp, with the subsequent divergence of colonizers in allopatry. The competitive coexistence of Corambe pacifica MacFarland & O'Donoghue, 1929 and Corambe steinbergae (Lance, 1962) off California is the result of independent colonization events. The closing of the Isthmus of Panama separated the latter species from a flock that have radiated within warm Atlantic waters since then. Our case study shows that morphological structures, if investigated in depth, bear the potential for an efficient phylogenetic analysis of groups that are still elusive to molecular analyses. Tracing character evolution and integrating a wide range of geographic, biological, and ecological background information allowed us to reconstruct an evolutionary scenario for corambids that is detailed and plausible, and can be tested by future molecular approaches. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163 , 585–604.     

Patterns and implications of extensive heterochrony in carnivoran cranial suture closure

Heterochronic changes in the rate or timing of development underpin many evolutionary transformations. In particular, the onset and rate of bone development have been the focus of many studies across large clades. In contrast, the termination of bone growth, as estimated by suture closure, has been studied far less frequently, although a few recent studies have shown this to represent a variable, although poorly understood, aspect of developmental evolution. Here, we examine suture closure patterns across 25 species of carnivoran mammals, ranging from social‐insectivores to hypercarnivores, to assess variation in suture closure across taxa, identify heterochronic shifts in a phylogenetic framework and elucidate the relationship between suture closure timing and ecology. Our results show that heterochronic shifts in suture closure are widespread across Carnivora, with several shifts identified for most major clades. Carnivorans differ from patterns identified for other mammalian clades in showing high variability of palatal suture closure, no correlation between size and level of suture closure, and little phylogenetic signal outside of musteloids. Results further suggest a strong influence of feeding ecology on suture closure pattern. Most of the species with high numbers of heterochronic shifts, such as the walrus and the aardwolf, feed on invertebrates, and these taxa also showed high frequency of closure of the mandibular symphysis, a state that is relatively rare among mammals. Overall, caniforms displayed more heterochronic shifts than feliforms, suggesting that evolutionary changes in suture closure may reflect the lower diversity of cranial morphology in feliforms.     

Patterns of heterochrony in the fossil record

Recent analyses of the fossil record have revealed that heterochrony has played a significant role in the evolution of most marine invertebrate groups. Recognition of several different heterochronic processes has allowed their influence under different ecological regimes to be assessed. Furthermore, recent research has demonstrated significant differences in frequencies of these processes between groups and at their different stages of phylogenetic development. The fossil record shows that heterochron y has been an important component in the generation of evolutionary trends. Heterochrony is an important factor in macroevolution because it can result in relatively abrupt morphological change with only minimum alteration of the genome.     

Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.     

THE ROLE OF HETEROCHRONY IN THE EVOLUTION OF CAMBRIAN TRILOBITES

1. Renewed interest in the role of changes to developmental regulation in organisms has highlighted the importance of heterochrony in the evolution of the Metazoa.
2. Beecher's interpretation of the evolution of the Trilobita as having been principally by peramorphosis is examined, as is the view of later workers, principally Stubblefield and Hupé, that paedomorphosis was a dominant factor in trilobite evolution.
3. Both peramorphosis and paedomorphosis are considered to have been important in trilobite evolution.
4. The role of paedomorphosis in the evolution of major morphological novelties is critically examined. Its importance in changes to the structure of the glabella is discussed and new terms proposed to describe the ontogenetic and phylogenetic state of the glabella.
5. The highly variable nature of early Cambrian trilobites, in particular the large degree of ontogenetic change, is considered, along with possible poor developmental control of the growth and moulting hormonal systems, to have been significant in providing a high degree of intrapopulational morphological variability. Selection of these heterochronic variants was responsible for the rapid diversification of the Trilobita during the Cambrian.     

Role of Caribbean Islands in the diversification and biogeography of Neotropical Heraclides swallowtails

Numerous hypotheses on the evolution of Neotropical biodiversity have stimulated research to provide a better understanding of diversity dynamics and distribution patterns of the region. However, few studies integrate molecular and morphological data with complete sampling of a Neotropical group, and so there has been little synthesis of the multiple processes governing biodiversity through space and time. Here, a total‐evidence phylogenetic approach is used to reconstruct the evolutionary history of the butterfly subgenus Heraclides. We used DNA sequences for two mitochondrial genes and one nuclear gene and coded 133 morphological characters of larvae and adults. A robust and well‐resolved phylogeny was obtained using several analytical approaches, while molecular dating and biogeographical analyses indicated an early Miocene origin (22 Mya) in the Caribbean Islands. We inferred six independent dispersal events from the Caribbean to the mainland, and three from the mainland to the Caribbean, and we suggest that cooling climates with decreasing sea levels may have contributed to these events. The time‐calibrated tree is best explained by a museum model of diversity in which both speciation and extinction rates remained constant through time. By assessing both continental and fine‐scale biodiversity patterns, this study provides new findings, for instance that islands may act as source of diversity rather than as a sink, to explain spatio‐temporal macroevolutionary processes within the Neotropical region.     

Skull osteology of Parvilacerta parva, a small-sized lacertid lizard from Asia Minor

The skull of the poorly known Asia Minor lacertid lizard Parvilacerta parva is described. In comparison to other palaearctic lacertids, Parvilacerta parva displays several peculiar traits such as a large braincase, a short parietal table, closed post-temporal openings, reduced ossification, or a large lacrimal. Many features are related to the small size of Parvilacerta parva and are of apparently heterochronic nature, as they can also be found in certain ontogenetic stages of other lacertid species. Small size and heterochrony even seem to be factors involved in the less-developed sexual dimorphism of Parvilacerta parva. The described morphology is interpreted to be related to a life history strategy in r-selecting, semiarid environments.     

Biogeography and evolution of Dolichandra (Bignonieae,Bignoniaceae)

Little information on evolutionary relationships of Neotropical organisms or on the factors that have shaped the diversity currently encountered in this region is available. However, it is clear that biotic interactions and abiotic aspects have played important roles for species diversification in the region. This study focuses on Dolichandra (Bignonieae, Bignoniaceae), a clade of Neotropical lianas that is distributed broadly across different habitats and with diverse pollination and dispersal systems. We used sequences from two plastid DNA markers (ndhF and rpl32‐trnL) and one nuclear gene (PepC) to infer phylogenetic relationships in Dolichandra using parsimony and Bayesian approaches. We then used this phylogenetic framework as basis to study the biogeographic history, reconstruct the evolution of morphological characters and test the impact of morphology and environment on the diversification of the genus. More specifically, we: (1) time‐calibrate the phylogenetic tree of Dolichandra; (2) estimate the ancestral areas of the various lineages; (3) estimate the ancestral states of discrete and continuous morphological traits; (4) test for phylogenetic signal in environmental and phenotypic data; and (5) test whether morphological characters and/or niche evolution are correlated with cladogenesis. All Dolichandra spp. are monophyletic in the combined molecular phylogeny; relationships among species are generally well resolved, although poorly supported in some instances. The genus is inferred to have originated 36.43–26.23 Mya, possibly in eastern South America. Ancestral state reconstructions of continuous and discrete floral characters inferred a mixed morphology as the ancestral condition for the group. Phylogenetic signal differed between perianth and sexual whorls and gradual evolution was recovered for all traits except style length and anther length. Environmental variables showed no phylogenetic signal and a pattern of variation that was not correlated with branch length, suggesting that environmental transitions were concomitant with speciation. Dispersal is inferred to be the main driver of the differential distribution observed among species. In addition, climatic preferences and floral characters seem to have been important reproductive barriers in Dolichandra. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 403–420.     

Convergent evolution in social swallows (Aves: Hirundinidae)

Behavioral shifts can initiate morphological evolution by pushing lineages into new adaptive zones. This has primarily been examined in ecological behaviors, such as foraging, but social behaviors may also alter morphology. Swallows and martins (Hirundinidae) are aerial insectivores that exhibit a range of social behaviors, from solitary to colonial breeding and foraging. Using a well‐resolved phylogenetic tree, a database of social behaviors, and morphological measurements, we ask how shifts from solitary to social breeding and foraging have affected morphological evolution in the Hirundinidae. Using a threshold model of discrete state evolution, we find that shifts in both breeding and foraging social behavior are common across the phylogeny of swallows. Solitary swallows have highly variable morphology, while social swallows show much less absolute variance in all morphological traits. Metrics of convergence based on both the trajectory of social lineages through morphospace and the overall morphological distance between social species scaled by their phylogenetic distance indicate strong convergence in social swallows, especially socially foraging swallows. Smaller physical traits generally observed in social species suggest that social species benefit from a distinctive flight style, likely increasing maneuverability and foraging success and reducing in‐flight collisions within large flocks. These results highlight the importance of sociality in species evolution, a link that had previously been examined only in eusocial insects and primates.     

The genetic control of heterochrony: Evidence from developmental mutants of Pisum sativum L.

Heterochrony, as a means of evolution in which the rate or timing of developmental events of the descendant is altered compared with that of the ancestor, is of significance because it suggests that rapid and dramatic morphological changes are possible with few genetic changes. The putative origin of plant taxa by this means of evolution is becoming increasingly frequent in the literature but there is little evidence of the extent of the genetic change necessary to alter the timing of developmental events to produce such changes. This study shows that the onset of flowering can be altered independently from the vegetative transition in leaf form in at least one genotype of Pisum in response to different environments. Further, it identifies 9 mutations that act in a heterochronic manner to produce dramatic morphological changes that can be described as progenesis, neoteny, hypermorphosis or acceleration. In addition, it is demonstrated that the same heterochronic process (e.g. progenesis) may be caused by genes controlling distinctly different physiological processes. It is suggested that Pisum is an ideal model species for studies of heterochrony and that few genetic changes are necessary to bring about dramatic heterochronic changes.     

Prey capture in lizards: differences in jaw–neck–forelimb coordination

Fish body muscles are arranged along the vertebral column in three‐dimensional W‐shaped blocks, called myomeres. Each myomere is separated from its neighbours by a collagenous sheet, the myoseptum, and embedded in these myosepta and in positions that are conserved throughout gnathostome evolution are distinct tendons. Within teleosts these tendons often ossify. Ossification is usually intramembranous but cartilaginous structures within the tendons have also been reported. Ossified myoseptal tendons are homologous to intermuscular bones and appear only in teleosts. The phylogenetic signal of myoseptal tendon ossfication has not been tested previously, although the presence and morphology of intermuscular bones have been used to infer phylogenetic relationships. We sample over a broad phylogenetic range of teleost fishes to test for (1) the effects of phylogenetic history on the presence of intermuscular bones and (2) morphological correlations with the presence of intermuscular bones. Body shape and fin position as well as vertebral number and aspect ratio are characters that are likely to affect the distribution of stresses along myoseptal tendons, and are therefore good functional predictors of myoseptal tendon ossification. We use the summary information by Patterson & Johnson for a list of species with intermuscular bones and reanalyse the homology of intermuscular bones to myoseptal tendons. We find that there is a phylogenetic signal in the distribution of four out of six ossified tendons, but that after correcting for phylogenetic relationships there are still morphological predictors for the presence of all ossified tendons. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 607–622.     

Tooth histology,attachment, and replacement in the Ichthyopterygia reviewed in an evolutionary context

Ichthyosaurs, an extinct group of Mesozoic marine diapsids, show a relatively small range of tooth crown morphologies. With few exceptions, members of the group bear a large number of conical teeth and show only minor heterodonty within a jaw. This uniformity in gross morphology masks a high degree of variation in both the quantity and arrangement of the mineralized tooth tissues. Here, we describe tooth tissue structure and distribution in derived ichthyosaurs. We synthesize these new observations with the historical literature, to map changes in the quantity and arrangement of tooth tissues. These changes affected tooth attachment, tooth replacement, plicidentine morphology, and the amount and distribution of cellular cementum. The amount of variation detected in features relating to ichthyosaurian dentition is not surprising given the geological longevity and morphological disparity of the group, but does emphasize the importance of extensive taxon sampling in studies of tooth histology and evolution. This study is important in that it incorporates morphological and histological information in a phylogenetic and developmental context, something that is rarely done for marine reptile dentitions.     

Evidence for heterochrony in the cranial evolution of fossil crocodyliforms

The southern supercontinent of Gondwana was home to an extraordinary diversity of stem‐crocodylians (Crocodyliformes) during the Late Cretaceous. The remarkable morphological disparity of notosuchian crocodyliforms indicates that this group filled a wide range of ecological roles more frequently occupied by other vertebrates. Among notosuchians, the distinctive cranial morphology and large body sizes of Baurusuchidae suggest a role as apex predators in ecosystems in which the otherwise dominant predatory theropod dinosaurs were scarce. Large‐bodied crocodyliforms, modern and extinct, are known to have reached large sizes by extending their growth period. In a similar way, peramorphic heterochronic processes may have driven the evolution of the similarly large baurusuchids. To assess the presence of peramorphic processes in the cranial evolution of baurusuchids, we applied a geometric morphometric approach to investigate ontogenetic cranial shape variation in a comprehensive sample of notosuchians. Our results provide quantitative morphological evidence that peramorphic processes influenced the cranial evolution of baurusuchids. After applying size and ancestral ontogenetic allometry corrections to our data, we found no support for the action of either hypermorphosis or acceleration, indicating that these two processes alone cannot explain the shape variation observed in Notosuchia. Nevertheless, the strong link between cranial shape variation and size increase in baurusuchids suggests that peramorphic processes were involved in the emergence of hypercarnivory in these animals. Our findings illustrate the role of heterochrony as a macroevolutionary driver, and stress, once more, the usefulness of geometric morphometric techniques for identifying heterochronic processes behind evolutionary trends.