COMPARATIVE PATTERNS OF CRANIOFACIAL DEVELOPMENT IN EUTHERIAN AND METATHERIAN MAMMALS

The sequence of differentiation of major elements of the skeletal, muscular and nervous systems of the head is examined in developmental series of five eutherian (placental) and four metatherian (marsupial) mammals. The analysis identifies the elements that are conserved across the Theria, those that are unique to the Metatheria and to the Eutheria, and those that are variable. It is shown that although there are slight shifts in the sequence of development within the somatic tissues of the head, the primary difference between marsupial and placental mammals involves the timing and rate of differentiation of structures of the central nervous system (CNS) relative to a specific subset of structures of the cranial skeleton and musculature. In eutherians, CNS morphogenesis is well underway before the somatic tissues of the head begin differentiation. In metatherians, CNS development is delayed considerably and certain elements of the skeletal and muscular systems are advanced. It is concluded that the developmental differences between marsupial and placental mammals are best explained by the interaction of several processes including neurogenesis as a potential rate-limiting step, the developmental requirements of somatic elements, and the extremely short period of organogenesis of marsupial mammals. Several other issues, including the way that these data may be applied to determine the primitive therian developmental condition, and the use of comparative developmental data to address basic questions on morphogenetic processes, are discussed.     

Levels of Homoplasy in the Evolution of the Mammalian Skeleton

It is commonly believed that there are differences in the evolutionary lability of the crania, dentition, and postcrania of mammals, the latter two being more prone to homoplasy because of strong selective pressures for feeding and locomotion, respectively. Further, because of the fragmentary nature of fossils, phylogenetic analyses of extinct taxa often must utilize characters based on only one of these systems. In this paper the levels of homoplasy (as measured by the consistency index; CI) were compared in characters based on these three anatomical systems in therian mammals. No statistically significant differences were found in the overall CIs of 41 data sets based on dental, cranial, or postcranial characters. Differences in homoplasy within data sets with two or three kinds of data were not statistically significant. These findings suggest that dental, cranial, and postcranial characters can be equally prone to homoplasy and none should be automatically dismissed, disregarded, or systematically weighted in phylogenetic analyses. The level of homoplasy in characters derived from a given region of the skeleton may differ depending on the taxonomic level of the taxa considered. Dental, cranial, and postcranial characters may not constitute natural classes, yet examination of the phylogenetic signal of these subsets of data previous to a simultaneous analysis can shed light on significant aspects of the evolutionary process.     

Phylogeny, diet, and cranial integration in australodelphian marsupials

Studies of morphological integration provide valuable information on the correlated evolution of traits and its relationship to long-term patterns of morphological evolution. Thus far, studies of morphological integration in mammals have focused on placentals and have demonstrated that similarity in integration is broadly correlated with phylogenetic distance and dietary similarity. Detailed studies have also demonstrated a significant correlation between developmental relationships among structures and adult morphological integration. However, these studies have not yet been applied to marsupial taxa, which differ greatly from placentals in reproductive strategy and cranial development and could provide the diversity necessary to assess the relationships among phylogeny, ecology, development, and cranial integration. This study presents analyses of morphological integration in 20 species of australodelphian marsupials, and shows that phylogeny is significantly correlated with similarity of morphological integration in most clades. Size-related correlations have a significant affect on results, particularly in Peramelia, which shows a striking decrease in similarity of integration among species when size is removed. Diet is not significantly correlated with similarity of integration in any marsupial clade. These results show that marsupials differ markedly from placental mammals in the relationships of cranial integration, phylogeny, and diet, which may be related to the accelerated development of the masticatory apparatus in marsupials.     

Comparing levels of homoplasy in the primate skeleton

Hard-tissue morphological characters (bones and teeth) are a primary source of information about the evolutionary history of primates. These tissues are commonly found as isolated elements in the fossil record and studied as three separate partitions: the dentition, the cranium, and the postcranium. The relative phylogenetic utility of characters from each partition is often called into question with respect to varying amounts of homoplasy. In this paper, the consistency index (CI) was used to measure levels of homoplasy in each data partition for a sample of fossil and living primates. Sources of bias in the collection and treatment of data and in the internal structure of the data set are addressed. These biases include number of taxa, number of characters, ordering of characters, amounts of polymorphically scored or missing data, and character-state distribution. The results of this study suggest that the levels of homoplasy are very similar, though the postcranial data may be slightly less homoplastic than either the dental or cranial data.     

Conserved relative timing of cranial ossification patterns in early mammalian evolution

We analyzed a comprehensive data set of ossification sequences including seven marsupial, 13 placental and seven sauropsid species. Data are provided for the first time for two major mammalian clades, Chiroptera and Soricidae, and for two rodent species; the published sequences of three species were improved with additional sampling. The relative timing of the onset of ossification in 17 cranial elements was recorded, resulting in 136 event pairs, which were treated as characters for each species. Half of these characters are constant across all taxa, 30% are variable but phylogenetically uninformative, and 19% potentially deliver diagnostic features for clades of two or more taxa. Using the conservative estimate of heterochronic changes provided by the program Parsimov, only a few heterochronies were found to diagnose mammals, marsupials, or placentals. A later onset of ossification of the pterygoid with respect to six other cranial bones characterizes therian mammals. This result may relate to the relatively small size of this bone in this clade. One change in relative onset of ossification is hypothesized as a potential human autapomorphy in the context of the sampling made: the earlier onset of the ossification of the periotic with respect to the lacrimal and to three basicranial bones. Using the standard error of scaled ranks across all species as a measure of each element's lability in developmental timing, we found that ossification of early, middle, and late events are similarly labile, with basicranial traits the most labile in timing of onset of ossification. Despite marsupials and placental mammals diverging at least 130 Ma, few heterochronic shifts in cranial ossification diagnose these clades.     

Gross brain morphology of Hypoptopomatinae and Neoplecostominae (Siluriformes: Loricariidae): Comparative anatomy and phylogenetic implications

Hypoptopomatinae and Neoplecostominae include about 250 valid species, a substantial portion of loricariid catfishes. Although the relationships among the members of these subfamilies have been inferred by many authors, the most recent hypotheses based on morphological and molecular data differ widely. Herein, we provide new data on the morphology of the central nervous system, and evaluate the usefulness of these characters in phylogenetic inference. To accomplish this, we characterized the gross brain morphology of those catfishes, and analyzed 54 neuroanatomical characters in a total of 40 terminal taxa representing Hypoptopomatinae and Neoplecostominae, and also members of Delturinae and Hypostominae as outgroups. Hypoptopomatinae and Neoplecostominae are recovered as separate subfamilies, and most of our results are compatible with morphology‐based analyses. We conclude that neuroanatomy provides an informative source of new characters with strong phylogenetic signal at all recovered taxonomic levels.     

Global interrelationships of Plesiosauria (Reptilia,Sauropterygia) and the pivotal role of taxon sampling in determining the outcome of phylogenetic analyses

Previous attempts to resolve plesiosaurian phylogeny are reviewed and a new phylogenetic data set of 66 taxa (67% of ingroup taxa examined directly) and 178 characters (eight new) is presented. We recover two key novel results: a monophyletic Plesiosauridae comprising Plesiosaurus dolichodeirus, Hydrorion brachypterygius, Microcleidus homalospondylus, Occitanosaurus tournemirensis and Seeleyosaurus guilelmiimperatoris; and five plesiosaurian taxa recovered outside the split between Plesiosauroidea and Pliosauroidea. These taxa are Attenborosaurus conybeari, ‘Plesiosaurus’macrocephalus and a clade comprising Archaeonectrus rostratus, Macroplata tenuiceps and BMNH 49202. Based on this result, a new name, Neoplesiosauria, is erected for the clade comprising Plesiosauroidea and Pliosauroidea. Taxon subsamples of the new dataset are used to simulate previous investigations of global plesiosaurian relationships. Based on these simulations, most major differences between previous global phylogenetic hypotheses can be attributed to differences in taxon sampling. These include the position of Leptocleididae and Polycotylidae and the monophyly or paraphyly of Rhomaleosauridae. On this basis we favour the results recovered by our, larger analysis. Leptocleididae and Polycotylidae are sister taxa, forming a monophyletic clade within Plesiosauroidea, indicating that the large‐headed, short‐necked ‘pliosauromorph’ body plan evolved twice within Plesiosauria. Rhomaleosauridae forms the monophyletic sister taxon of Pliosauridae within Pliosauroidea. Problems are identified with previous phylogenetic definitions of plesiosaurian clades and new, stem‐based definitions are presented that should maintain their integrity over a range of phylogenetic hypotheses. New, rank‐free clade names Cryptoclidia and Leptocleidia are erected to replace the superfamilies Cryptoclidoidea and Leptocleidoidea. These were problematic as they were nested within the superfamily Plesiosauroidea. The incongruence length difference test indicates no significant difference in levels of homoplasy between cranial and postcranial characters.     

THE AUDITORY REGION OF EARLY PALEOCENE PUCADELPHYDAE (MAMMALIA, METATHERIA) FROM TIUPAMPA, BOLIVIA, WITH PHYLOGENETIC IMPLICATIONS

Abstract:  New petrosal bones, assigned to Pucadelphys and Andinodelphys , from the Lower Paleocene of Tiupampa, Bolivia, are described. These remains provide new information on the anatomy of the ear region of these taxa. The re-examination of characters from the petrosal and basicranium shed light on the phylogenetic relationships of the three Tiupampan genera known from complete cranial remains (i.e. Mayulestes , Pucadelphys and Andinodelphys ). The combination of dental, general cranial and basicranial characters led to two alternative hypotheses. The first is that borhyaenoids (including Mayulestes ) are nested within Notometatheria. Pucadelphyds (i.e. Pucadelphys and Andinodelphys ) are the sister group of a clade comprising MHNC 8369 (one isolated petrosal from Tiupampa) and Marsupialia. The second favours the paraphyly of 'borhyaenoids' (i.e. the exclusion of Mayulestes from borhyaenoids) and the polyphyly of 'Notometatheria'. In this case, Mayulestes and borhyaenids represent the stem group of a clade including Asiatic, American and Australian metatherians. This analysis of combined datasets (dental, general cranial and basicranial) highlighted contradictory information in the dental and cranial characters, serving to emphasize that in a large anatomical complex like an entire skull mosaic evolution of the characters is likely.     

Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships

The affinities of three problematic groups of elongate, burrowing reptiles (amphisbaenians, dibamids and snakes) are reassessed through a phylogenetic analysis of all the major groups of squamates, including the important fossil taxa Sineoamphisbaena, mosasauroids and Pachyrhachis; 230 phylogenetically informative osteological characters were evaluated in 22 taxa. Snakes (including Pachyrhachis) are anguimorphs, being related firstly to large marine mosasauroids, and secondly to monitor lizards (varanids). Scincids and cordylids are not related to lacertiforms as previously thought, but to anguimorphs. Amphisbaenians and dibamids are closely related, and Sineoamphisbaena is the sister group to this clade. The amphisbaenian-dibamid-Sineoamphisbaena clade, in turn, is related to gekkotans and xantusiids. When the fossil taxa are ignored, snakes, amphisbaenians and dibamids form an apparently well-corroborated clade nested within anguimorphs. However, nearly all of the characters supporting this arrangement are correlated with head-first burrowing (miniaturization, cranial consolidation, body elongation, limb reduction), and invariably co-occur in other tetrapods with similar habits. These characters are potentially very misleading because of their sheer number and because they largely represent reductions or losses. It takes very drastic downweighting of these linked characters to alter tree topology: if fossils are excluded from the analysis, a (probably spurious) clade consisting of elongate, fossorial taxa almost always results. These results underscore the importance of including all relevant taxa in phylogenetic analyses. Inferring squamate phylogeny depends critically on the inclusion of certain (fossil) taxa with combinations of character states that demonstrate convergent evolution of the elongate, fossorial ecomorph in amphisbaenians and dibamids, and in snakes. In the all-taxon analysis, the position of snakes within anguimorphs is more strongly-corroborated than the association of amphisbaenians and dibamids with gekkotans. When the critical fossil taxa are deleted, snakes ‘attract’ the amphisbaenian-dibamid clade on the basis of a suite of correlated characters. While snakes remain anchored in anguimorphs, the amphisbaenian-dibamid clade moves away from gekkotans to join them. Regardless of the varying positions of the three elongate burrowing taxa, the interrelationships between the remaining limbed squamates (‘lizards’) are constant; thus, the heterodox affinities of scincids, cordylids, and xantusiids identified in this analysis appear to be robust. Finally, the position of Pachyrhachis as a basal snake rather than (as recently suggested) a derived snake is supported on both phylogenetic and evolutionary grounds.     

Using Phylogenies to Study Convergence: The Case of the Ant-Eating Mammals

Identifying when homoplasy is due to convergence requires confidencein trees and precise analysis of potentially convergent characters.Some features of mammals that eat mostly ants and termites areused as examples of convergence; the most speciose assemblagesof these mammals are in the orders Xenarthra and Pholidota.My studies on cranial muscles in xenarthrans and pholidotansaim to 1) precisely describe the anatomy in ant-eating and non-ant-eatinglineages, 2) assess variation among ant-eating lineages, and3) compare the most derived conditions (in xenarthran anteatersand pholidotan pangolins). These data clarify the nature ofmorphological adaptation in ant-eating mammals, and when combinedwith accumulating phylogenetic studies, allow us to distinguishfeatures that have evolved convergently from those that arevariable but not correlated with diet. Interpreting the extremesimilarity in anteaters and pangolins remains problematic dueto lingering disagreement among phylogenetic hypotheses. Prevailingopinion favors interpretation of these similarities as convergent.     

Are Cranial Biomechanical Simulation Data Linked to Known Diets in Extant Taxa? A Method for Applying Diet-Biomechanics Linkage Models to Infer Feeding Capability of Extinct Species

Performance of the masticatory system directly influences feeding and survival, so adaptive hypotheses often are proposed to explain craniodental evolution via functional morphology changes. However, the prevalence of “many-to-one” association of cranial forms and functions in vertebrates suggests a complex interplay of ecological and evolutionary histories, resulting in redundant morphology-diet linkages. Here we examine the link between cranial biomechanical properties for taxa with different dietary preferences in crown clade Carnivora, the most diverse clade of carnivorous mammals. We test whether hypercarnivores and generalists can be distinguished based on cranial mechanical simulation models, and how such diet-biomechanics linkages relate to morphology. Comparative finite element and geometric morphometrics analyses document that predicted bite force is positively allometric relative to skull strain energy; this is achieved in part by increased stiffness in larger skull models and shape changes that resist deformation and displacement. Size-standardized strain energy levels do not reflect feeding preferences; instead, caniform models have higher strain energy than feliform models. This caniform-feliform split is reinforced by a sensitivity analysis using published models for six additional taxa. Nevertheless, combined bite force-strain energy curves distinguish hypercarnivorous versus generalist feeders. These findings indicate that the link between cranial biomechanical properties and carnivoran feeding preference can be clearly defined and characterized, despite phylogenetic and allometric effects. Application of this diet-biomechanics linkage model to an analysis of an extinct stem carnivoramorphan and an outgroup creodont species provides biomechanical evidence for the evolution of taxa into distinct hypercarnivorous and generalist feeding styles prior to the appearance of crown carnivoran clades with similar feeding preferences.     

Assessment of available anatomical characters for linking living mammals to fossil taxa in phylogenetic analyses

Analyses of living and fossil taxa are crucial for understanding biodiversity through time. The total evidence method allows living and fossil taxa to be combined in phylogenies, using molecular data for living taxa and morphological data for living and fossil taxa. With this method, substantial overlap of coded anatomical characters among living and fossil taxa is vital for accurately inferring topology. However, although molecular data for living species are widely available, scientists generating morphological data mainly focus on fossils. Therefore, there are fewer coded anatomical characters in living taxa, even in well-studied groups such as mammals. We investigated the number of coded anatomical characters available in phylogenetic matrices for living mammals and how these were phylogenetically distributed across orders. Eleven of 28 mammalian orders have less than 25% species with available characters; this has implications for the accurate placement of fossils, although the issue is less pronounced at higher taxonomic levels. In most orders, species with available characters are randomly distributed across the phylogeny, which may reduce the impact of the problem. We suggest that increased morphological data collection efforts for living taxa are needed to produce accurate total evidence phylogenies.     

Missing data,incomplete taxa,and phylogenetic accuracy

The problem of missing data is often considered to be the most important obstacle in reconstructing the phylogeny of fossil taxa and in combining data from diverse characters and taxa for phylogenetic analysis. Empirical and theoretical studies show that including highly incomplete taxa can lead to multiple equally parsimonious trees, poorly resolved consensus trees, and decreased phylogenetic accuracy. However, the mechanisms that cause incomplete taxa to be problematic have remained unclear. It has been widely assumed that incomplete taxa are problematic because of the proportion or amount of missing data that they bear. In this study, I use simulations to show that the reduced accuracy associated with including incomplete taxa is caused by these taxa bearing too few complete characters rather than too many missing data cells. This seemingly subtle distinction has a number of important implications. First, the so-called missing data problem for incomplete taxa is, paradoxically, not directly related to their amount or proportion of missing data. Thus, the level of completeness alone should not guide the exclusion of taxa (contrary to common practice), and these results may explain why empirical studies have sometimes found little relationship between the completeness of a taxon and its impact on an analysis. These results also (1) suggest a more effective strategy for dealing with incomplete taxa, (2) call into question a justification of the controversial phylogenetic supertree approach, and (3) show the potential for the accurate phylogenetic placement of highly incomplete taxa, both when combining diverse data sets and when analyzing relationships of fossil taxa.