Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates

Many animals are active only during a particular time (e.g., day vs. night), a partitioning that may have important consequences for species coexistence. An open question is the extent to which this diel activity niche is evolutionarily conserved or labile. Here, we analyze diel activity data across a phylogeny of 1914 tetrapod species. We find strong phylogenetic signal, showing that closely related species tend to share similar activity patterns. Ancestral reconstructions show that nocturnality was the most likely ancestral diel activity pattern for tetrapods and many major clades within it (e.g., amphibians, mammals). Remarkably, nocturnal activity appears to have been maintained continuously in some lineages for ～350 million years. Thus, we show that traits involved in local‐scale resource partitioning can be conserved over strikingly deep evolutionary time scales. We also demonstrate a potentially important (but often overlooked) metric of niche conservatism. Finally, we show that diurnal lineages appear to have faster speciation and diversification rates than nocturnal lineages, which may explain why there are presently more diurnal tetrapod species even though diurnality appears to have evolved more recently. Overall, our results may have implications for studies of community ecology, species richness, and the evolution of diet and communication systems.     

Limb development in a "nonmodel" vertebrate, the direct-developing frog Eleutherodactylus coqui.

Mechanisms that mediate limb development are regarded as highly conserved among vertebrates, especially tetrapods. Yet, this assumption is based on the study of relatively few species, and virtually none of those that display any of a large number of specialized life-history or reproductive modes, which might be expected to affect developmental pattern or process. Direct development is an alternative life history found in many anuran amphibians. Many adult features that form after hatching in metamorphic frogs, such as limbs, appear during embryogenesis in direct-developing species. Limb development in the direct-developing frog Eleutherodactylus coqui presents a mosaic of apparently conserved and novel features. The former include the basic sequence and pattern of limb chondrogenesis, which are typical of anurans generally and appear largely unaffected by the gross shift in developmental timing; expression of Distal-less protein (Dlx) in the distal ectoderm; expression of the gene Sonic hedgehog (Shh) in the zone of polarizing activity (ZPA); and the ability of the ZPA to induce supernumerary digits when transplanted to the anterior region of an early host limb bud. Novel features include the absence of a morphologically distinct apical ectodermal ridge, the ability of the limb to continue distal outgrowth and differentiation following removal of the distal ectoderm, and earlier cessation of the inductive ability of the ZPA. Attempts to represent tetrapod limb development as a developmental "module" must allow for this kind of evolutionary variation among species.     

Biogeography of Triassic tetrapods: evidence for provincialism and driven sympatric cladogenesis in the early evolution of modern tetrapod lineages

Triassic tetrapods are of key importance in understanding their evolutionary history, because several tetrapod clades, including most of their modern lineages, first appeared or experienced their initial evolutionary radiation during this Period. In order to test previous palaeobiogeographical hypotheses of Triassic tetrapod faunas, tree reconciliation analyses (TRA) were performed with the aim of recovering biogeographical patterns based on phylogenetic signals provided by a composite tree of Middle and Late Triassic tetrapods. The TRA found significant evidence for the presence of different palaeobiogeographical patterns during the analysed time spans. First, a Pangaean distribution is observed during the Middle Triassic, in which several cosmopolitan tetrapod groups are found. During the early Late Triassic a strongly palaeolatitudinally influenced pattern is recovered, with some tetrapod lineages restricted to palaeolatitudinal belts. During the latest Triassic, Gondwanan territories were more closely related to each other than to Laurasian ones, with a distinct tetrapod fauna at low palaeolatitudes. Finally, more than 75 per cent of the cladogenetic events recorded in the tetrapod phylogeny occurred as sympatric splits or within-area vicariance, indicating that evolutionary processes at the regional level were the main drivers in the radiation of Middle and Late Triassic tetrapods and the early evolution of several modern tetrapod lineages.     

The phylogenetic relationship of tetrapod, coelacanth, and lungfish revealed by the sequences of forty-four nuclear genes

The origin of tetrapods is a major outstanding issue in vertebrate phylogeny. Each of the three possible principal hypotheses (coelacanth, lungfish, or neither being the sister group of tetrapods) has found support in different sets of data. In an attempt to resolve the controversy, sequences of 44 nuclear genes encoding amino acid residues at 10,404 positions were obtained and analyzed. However, this large set of sequences did not support conclusively one of the three hypotheses. Apparently, the coelacanth, lungfish, and tetrapod lineages diverged within such a short time interval that at this level of analysis, their relationships appear to be an irresolvable trichotomy.     

Ecophysiological steps of marine adaptation in extant and extinct non-avian tetrapods

Marine reptiles and mammals are phylogenetically so distant from each other that their marine adaptations are rarely compared directly. We reviewed ecophysiological features in extant non-avian marine tetrapods representing 31 marine colonizations to test whether there is a common pattern across higher taxonomic groups, such as mammals and reptiles. Marine adaptations in tetrapods can be roughly divided into aquatic and haline adaptations, each of which seems to follow a sequence of three steps. In combination, these six categories exhibit five steps of marine adaptation that apply across all clades except snakes: Step M1, incipient use of marine resources; Step M2, direct feeding in the saline sea; Step M3, water balance maintenance without terrestrial fresh water; Step M4, minimized terrestrial travel and loss of terrestrial feeding; and Step M5, loss of terrestrial thermoregulation and fur/plumage. Acquisition of viviparity is not included because there is no known case where viviparity evolved after a tetrapod lineage colonized the sea. A similar sequence is found in snakes but with the haline adaptation step (Step M3) lagging behind aquatic adaptation (haline adaptation is Step S5 in snakes), most likely because their unique method of water balance maintenance requires a supply of fresh water. The same constraint may limit the maximum body size of fully marine snakes. Steps M4 and M5 in all taxa except snakes are associated with skeletal adaptations that are mechanistically linked to relevant ecophysiological features, allowing assessment of marine adaptation steps in some fossil marine tetrapods. We identified four fossil clades containing members that reached Step M5 outside of stem whales, pinnipeds, sea cows and sea turtles, namely Eosauropterygia, Ichthyosauromorpha, Mosasauroidea, and Thalattosuchia, while five other clades reached Step M4: Saurosphargidae, Placodontia, Dinocephalosaurus, Desmostylia, and Odontochelys. Clades reaching Steps M4 and M5, both extant and extinct, appear to have higher species diversity than those only reaching Steps M1 to M3, while the total number of clades is higher for the earlier steps. This suggests that marine colonizers only diversified greatly after they minimized their use of terrestrial resources, with many lineages not reaching these advanced steps. Historical patterns suggest that a clade does not advance to Steps M4 and M5 unless these steps are reached early in the evolution of the clade. Intermediate forms before a clade reached Steps M4 and M5 tend to become extinct without leaving extant descendants or fossil evidence. This makes it difficult to reconstruct the evolutionary history of marine adaptation in many clades. Clades that reached Steps M4 and M5 tend to last longer than other marine tetrapod clades, sometimes for more than 100 million years.     

Trophic convergence drives morphological convergence in marine tetrapods

Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets—even across large phylogenetic distances—are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.     

Radiation and functional diversification of alpha keratins during early vertebrate evolution

The conquest of land was arguably one of the most fundamental ecological transitions in vertebrates and entailed significant changes in skin structure and appendages to cope with the new environment. In extant tetrapods, the rigidity of the integument is largely created by type I and type II keratins, which are structural proteins essential in forming a strong cytoplasmic network. It is expected that such proteins have undergone fundamental changes in both stem and crown tetrapods. Here, we integrate genomic, phylogenetic, and expression data in a comprehensive study on the early evolution and functional diversification of tetrapod keratins. Our analyses reveal that all type I and type II tetrapod keratins evolved from only two genes that were present in the ancestor of extant vertebrates. Subsequently, the water-to-land transition in the stem lineage of tetrapods was associated with a major radiation and functional diversification of keratin genes. These duplications acquired functions that serve rigidity in integumental hard structures and were the prime for subsequent independent keratin diversification in tetrapod lineages.     

Mass extinctions among tetrapods and the quality of the fossil record

The fossil record of tetrapods is very patchy because of the problems of preservation, in terrestrial sediments in particular, and because vertebrates are rarely very abundant. However, the fossil record of tetrapods has the advantages that it is easier to establish a phylogenetic taxonomy than for many invertebrate groups, and there is the potential for more detailed ecological analyses. The relative incompleteness of a fossil record may be assessed readily, and this can be used to test whether drops in overall diversity are related to mass extinctions or to gaps in our knowledge. Absolute incompleteness cannot be assessed directly, but a historical approach may offer clues to future improvements in our knowledge. One of the key problems facing palaeobiologists is paraphyly, the fact that many higher taxa in common use do not contain all of the descendants of the common ancestor. This may be overcome by cladistic analysis and the identification of monophyletic groups. The diversity of tetrapods increased from the Devonian to the Permian, remained roughly constant during the Mesozoic, and then began to increase in the late Cretaceous, and continued to do so during the Tertiary. The rapid radiation of 'modern' tetrapod groups--frogs, salamanders, lizards, snakes, turtles, crocodilians, birds and mammals--was hardly affected by the celebrated end-Cretaceous extinction event. Major mass extinctions among tetrapods took place in the early Permian, late Permian, early Triassic, late Triassic, late Cretaceous, early Oligocene and late Miocene. Many of these events appear to coincide with the major mass extinctions among marine invertebrates, but the tetrapod record is largely equivocal with regard to the theory of periodicity of mass extinctions.     

Fish fingers: digit homologues in sarcopterygian fish fins

A defining feature of tetrapod evolutionary origins is the transition from fish fins to tetrapod limbs. A major change during this transition is the appearance of the autopod (hands, feet), which comprises two distinct regions, the wrist/ankle and the digits. When the autopod first appeared in Late Devonian fossil tetrapods, it was incomplete: digits evolved before the full complement of wrist/ankle bones. Early tetrapod wrists/ankles, including those with a full complement of bones, also show a sharp pattern discontinuity between proximal elements and distal elements. This suggests the presence of a discontinuity in the proximal-distal sequence of development. Such a discontinuity occurs in living urodeles, where digits form before completion of the wrist/ankle, implying developmental independence of the digits from wrist/ankle elements. We have observed comparable independent development of pectoral fin radials in the lungfish Neoceratodus (Osteichthyes: Sarcopterygii), relative to homologues of the tetrapod limb and proximal wrist elements in the main fin axis. Moreover, in the Neoceratodus fin, expression of Hoxd13 closely matches late expression patterns observed in the tetrapod autopod. This evidence suggests that Neoceratodus fin radials and tetrapod digits may be patterned by shared mechanisms distinct from those patterning the proximal fin/limb elements, and in that sense are homologous. The presence of independently developing radials in the distal part of the pectoral (and pelvic) fin may be a general feature of the Sarcopterygii.     

Digit reduction, body size, and paedomorphosis in salamanders

SUMMARY The loss of digits is a widespread evolutionary trend in tetrapods which occurs in nearly every major clade. Alberch and Gale showed that the order in which digits are evolutionarily lost in salamanders versus frogs corresponds to the order in which they develop in each group, providing a classic example of developmental constraint. However, what actually drives the loss of digits in salamanders has remained unclear. Alberch and Gale suggested that loss of digits might be associated with paedomorphosis or with reduced body size. We test these hypotheses by combining morphometric and phylogenetic information for 98 species of salamanders. We find that digit loss is associated with both paedomorphosis and reduction in body size. However, these trends are surprisingly contradictory, in that paedomorphosis is significantly associated with an increase in body size in salamanders. Thus, much of the extreme digit reduction is found in the smaller species within paedomorphic clades that have, on average, unusually large body size. Our results show that the consequences of changes in body size on morphology are highly context dependent. We also show (possibly for the first time) a significant association between paedomorphosis and increased body size, rather than the expected association with reduced body size.     

Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development

The tetrapod limb, which has served as a paradigm for the study of development and morphological evolution, is becoming a paradigm for developmental evolution as well. In its origin and diversification, the tetrapod limb has undergone a great deal of remodeling. These morphological changes and other evolutionary phenomena have produced variation in mechanisms of tetrapod limb development. Here, we review that variation in the four major clades of limbed tetrapods. Comparisons in a phylogenetic context reveal details of development and evolution that otherwise may have been unclear. Such details include apparent differences in the mechanisms of dorsal-ventral patterning and limb identity specification between mouse and chick and mechanistic novelties in amniotes, anurans, and urodeles. As we gain a better understanding of the details of limb development, further differences among taxa will be revealed. The use of appropriate comparative techniques in a phylogenetic context thus sheds light on evolutionary transitions in limb morphology and the generality of developmental models across species and is therefore important to both evolutionary and developmental biologists.     

Interpreting the autopodia of tetrapods: interphalangeal lines hinge on too many assumptions

Recently Peters proposed the concept of ‘interphalangeal lines’, defined as sub-parallel lines that could supposedly be drawn across the joints of the digits of all tetrapods. The lines were viewed as potential axes of rotation, and it was suggested that they could be used to determine the resting position of the digits, reconstruct missing digital elements of fossil tetrapods, and provide information on systematic relationships. Evidence was adduced from the skeletons of recent and fossil vertebrates and from footprints. However, detailed analysis shows that these claims are largely unfounded. Linear alignments of joints on neighbouring digits are not consistently present in tetrapods, especially across locomotor cycles. Even if present, interphalangeal (IP) lines would rarely be in an appropriate orientation to facilitate joint movements during locomotion. There is no reason to believe that IP lines would be homologous across different taxa, so they cannot be used to infer systematic relationships. Finally, the alleged support from the ichnological record is undermined by the uncertain relationship between the joint structure of the skeleton and the form of the print. We conclude that IP lines cannot be consistently constructed on tetrapod extremities, and would have minimal functional relevance or predictive power in any case.     

Fins to limbs: what the fossils say

A broad phylogenetic review of fins, limbs, and girdles throughout the stem and base of the crown group is needed to get a comprehensive idea of transformations unique to the assembly of the tetrapod limb ground plan. In the lower part of the tetrapod stem, character state changes at the pectoral level dominate; comparable pelvic level data are limited. In more crownward taxa, pelvic level changes dominate and repeatedly precede similar changes at pectoral level. Concerted change at both levels appears to be the exception rather than the rule. These patterns of change are explored by using afternative treatments of data in phylogenetic analyses. Results highlight a large data gap in the stem group preceding the first appearance of limbs with digits. It is also noted that the record of morphological diversity among stem tetrapods is somewhat worse than that of basal crown group tetrapods. The pre-limbed evolution of stem tetrapod paired fins is marked by a gradual reduction in axial segment numbers (mesomeres); pectoral fins of the sister group to limbed tetrapods include only three. This reduction in segment number is accompanied by increased regional specialization, and these changes are discussed with reference to the phylogenetic distribution of characteristics of the stylopod, zeugopod, and autopod.     

Relationship among coelacanths,lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

To clarify the relationship among coelacanths, lungfishes, and tetrapods, the amino acid sequences deduced from the nucleotide sequences of mitochondrial cytochrome oxidase subunit I (COI) genes were compared. The phylogenetic tree of these animals, including the coelacanth Latimeria chalumnae and the lungfish Lepidosiren paradoxa, was inferred by several methods. These analyses consistently indicate a coelacanth/lungfish clade, to which little attention has been paid by previous authors with the exception of some morphologists. Overall evidence of other mitochondrial genes reported previously and the results of this study equally support the coelacanth/lungfish and lungfish/tetrapod clades, ruling out the coelacanth/tetrapod clade.Correspondence to: K. Watanabe 0592     

Understanding angiosperm diversification using small and large phylogenetic trees

How will the emerging possibility of inferring ultra-large phylogenies influence our ability to identify shifts in diversification rate? For several large angiosperm clades (Angiospermae, Monocotyledonae, Orchidaceae, Poaceae, Eudicotyledonae, Fabaceae, and Asteraceae), we explore this issue by contrasting two approaches: (1) using small backbone trees with an inferred number of extant species assigned to each terminal clade and (2) using a mega-phylogeny of 55473 seed plant species represented in GenBank. The mega-phylogeny approach assumes that the sample of species in GenBank is at least roughly proportional to the actual species diversity of different lineages, as appears to be the case for many major angiosperm lineages. Using both approaches, we found that diversification rate shifts are not directly associated with the major named clades examined here, with the sole exception of Fabaceae in the GenBank mega-phylogeny. These agreements are encouraging and may support a generality about angiosperm evolution: major shifts in diversification may not be directly associated with major named clades, but rather with clades that are nested not far within these groups. An alternative explanation is that there have been increased extinction rates in early-diverging lineages within these clades. Based on our mega-phylogeny, the shifts in diversification appear to be distributed quite evenly throughout the angiosperms. Mega-phylogenetic studies of diversification hold great promise for revealing new patterns, but we will need to focus more attention on properly specifying null expectation.     

Searching for the closest living relative(s) of tetrapods through evolutionary analyses of mitochondrial and nuclear data

The phylogenetic relationships of the African lungfish (Protopterus dolloi) and the coelacanth (Latimeria chalumnae) with respect to tetrapods were analyzed using complete mitochondrial genome DNA sequences. A lungfish + coelancanth clade was favored by maximum parsimony (although this result is dependent on which transition:transversion weights are applied), and a lungfish + tetrapod clade was supported by neighbor-joining and maximum-likelihood analyses. These two hypotheses received the strongest statistical and bootstrap support to the exclusion of the third alternative, the coelacanth + tetrapod sister group relationship. All mitochondrial protein coding genes combined favor a lungfish + tetrapod grouping. We can confidently reject the hypothesis that the coelacanth is the closest living relative of tetrapods. When the complete mitochondrial sequence data were combined with nuclear 28S rRNA gene data, a lungfish + coelacanth clade was supported by maximum parsimony and maximum likelihood, but a lungfish + tetrapod clade was favored by neighbor-joining. The seeming conflicting results based on different data sets and phylogenetic methods were typically not statistically strongly supported based on Kishino-Hasegawa and Templeton tests, although they were often supported by strong bootstrap values. Differences in rate of evolution of the different mitochondrial genes (slowly evolving genes such as the cytochrome oxidase and tRNA genes favored a lungfish + coelacanth clade, whereas genes of relatively faster substitution rate, such as several NADH dehydrogenase genes, supported a lungfish + tetrapod grouping), as well as the rapid radiation of the lineages back in the Devonian, rather than base compositional biases among taxa seem to be directly responsible for the remaining uncertainty in accepting one of the two alternate hypotheses.     

Proposed habitats of early tetrapods: gills, kidneys, and the water-land transition

Recent finds of early tetrapods have established that the most primitive form, Acanthostega, retained internal gills and other fish-like features; this has led to the conclusion that it was a primarily aquatic animal. Other Late Devonian tetrapods, such as lchthyostega and Tulerpeton, provide no evidence of internal gills, but have also been interpreted as inhabiting an aquatic environment. The probable aquatic habits of a diversity of Devonian tetrapods has led to the suggestion that the entire early tetrapod radiation may have been an aquatic one, with terrestriality having evolved in later forms. However, consideration of the physiology of living amphibious vertebrates suggests that this scenario is unlikely. The use of the gills for the excretion of carbon dioxide and ammonia appears to be a fundamental feature of all primarily aquatic vertebrates. No living fish loses its internal gills, even if it excretes a significant portion of its nitrogenous waste as urea via the kidney in the water. Gills are simply too valuable to be lost by an aquatic animal, even in those air-breathing fishes that no longer use the gills for oxygen uptake. We suggest that the apparent loss of the gills in tetrapods more derived than Acanthostega signals their descent from a more terrestrial phase in tetrapod evolution, following the primary assumption by the kidney of the excretion of nitrogenous wastes. Without this new role of the kidney, loss of the gills would have been impossible. With this new kidney role, loss of the gills may have been advantageous in reducing desiccation on land.     

Molecular phylogeny reveals extensive ancient and ongoing radiations in a snapping shrimp species complex (Crustacea,Alpheidae, Alpheus armillatus)

Tropical marine habitats often harbor high biodiversity, including many cryptic taxa. Though the prevalence of cryptic marine taxa is well known, the evolutionary histories of these groups remain poorly understood. The snapping shrimp genus Alpheus is a good model for such investigations, as cryptic species complexes are very common, indicating widespread genetic diversification with little or no morphological change. Here, we present an extensive phylogeographic investigation of the diversified amphi-American Alpheus armillatus species complex, with geographic sampling in the Caribbean Sea, Gulf of Mexico, Florida, Brazil, and the tropical Eastern Pacific. Sequence data from two mitochondrial genes (16SrRNA and cytochrome oxidase I) and one nuclear gene (myosin heavy chain) provide strong evidence for division of the species complex into six major clades, with extensive substructure within each clade. Our total data set suggests that the A. armillatus complex includes no less than 19 putative divergent lineages, 11 in the Western Atlantic and 8 in the Eastern Pacific. Estimates of divergence times from Bayesian analyses indicate that the radiation of the species complex began ～10 MYA with the most recent divergences among subclades dating to within the last 3 MY. Furthermore, individuals from the six major clades had broadly overlapping geographic distributions, which may reflect secondary contact among previously isolated lineages, and have apparently undergone several changes in superficial coloration, which is typically the most pronounced phenotypic character distinguishing lineages. In addition, the extensive substructure within clades indicates a great deal of molecular diversification following the rise of the Isthmus of Panama. In summary, this investigation reflects substantial biodiversity concealed by morphological similarity, and suggests that both ancient and ongoing divergences have contributed to the generation of this biodiversity. It also underlines the necessity to work with the most complete data set possible, which includes comprehensive and wide-ranging sampling of taxa.     

DEVELOPMENTAL BASIS OF TOOTHLESSNESS IN TURTLES: INSIGHT INTO CONVERGENT EVOLUTION OF VERTEBRATE MORPHOLOGY

The tooth is a major component of the vertebrate feeding apparatus and plays a crucial role in species survival, thus subjecting tooth developmental programs to strong selective constraints. However, irrespective of their functional importance, teeth have been lost in multiple lineages of tetrapod vertebrates independently. To understand both the generality and the diversity of developmental mechanisms that cause tooth agenesis in tetrapods, we investigated expression patterns of a series of tooth developmental genes in the lower jaw of toothless turtles and compared them to that of toothed crocodiles and the chicken as a representative of toothless modern birds. In turtle embryos, we found impairment of Shh signaling in the oral epithelium and early‐stage arrest of odontoblast development caused by termination of Msx2 expression in the dental mesenchyme. Our data indicate that such changes underlie tooth agenesis in turtles and suggest that the mechanism that leads to early‐stage odontogenic arrest differs between birds and turtles. Our results demonstrate that the cellular and molecular mechanisms that regulate early‐stage arrest of tooth development are diverse in tetrapod lineages, and odontogenic developmental programs may respond to changes in upstream molecules similarly thereby evolving convergently with feeding morphology.     

Elbow joint adductor moment arm as an indicator of forelimb posture in extinct quadrupedal tetrapods

Forelimb posture has been a controversial aspect of reconstructing locomotor behaviour in extinct quadrupedal tetrapods. This is partly owing to the qualitative and subjective nature of typical methods, which focus on bony articulations that are often ambiguous and unvalidated postural indicators. Here we outline a new, quantitatively based forelimb posture index that is applicable to a majority of extant tetrapods. By determining the degree of elbow joint adduction/abduction mobility in several tetrapods, the carpal flexor muscles were determined to also play a role as elbow adductors. Such adduction may play a major role during the stance phase in sprawling postures. This role is different from those of upright/sagittal and sloth-like creeping postures, which, respectively, depend more on elbow extensors and flexors. Our measurements of elbow muscle moment arms in 318 extant tetrapod skeletons (Lissamphibia, Synapsida and Reptilia: 33 major clades and 263 genera) revealed that sprawling, sagittal and creeping tetrapods, respectively, emphasize elbow adductor, extensor and flexor muscles. Furthermore, scansorial and non-scansorial taxa, respectively, emphasize flexors and extensors. Thus, forelimb postures of extinct tetrapods can be qualitatively classified based on our quantitative index. Using this method, we find that Triceratops (Ceratopsidae), Anhanguera (Pterosauria) and desmostylian mammals are categorized as upright/sagittally locomoting taxa.