Evolution and functional significance of tendon ossification in woodcreepers (Aves: Passeriformes: Dendrocolaptinae)

The woodcreepers, a clade of scansorial, neotropical birds, are distinctive among passerines in having extensive tendon ossification. Dissection of 42 of the 50 species indicates that such ossification in the hindlimb is limited almost entirely to tendons of insertion of the crural muscles. Most crural muscles have ossifications, and in all but one the ossified tendons are long and thin. Preliminary dissection revealed a similar pattern among ossified wing tendons. Phylogenetic analysis suggests that extensive tendon ossification is a synapomorphy of the woodcreepers. The species of Dendrocincla, which form a clade, show secondary reduction of ossification in some tendons, which may be correlated with increased intraspecific variation and with an expansion of foraging habits and postures to include nonscansorial behaviors. In contrast, the larger woodcreepers, other than Drymornis bridgesii and Nasica longirostris, form a clade with virtually no loss in ossification or evidence of intraspecific variation, even in large series of two species. Phylogenetic losses do not occur for the primary flexor of the ankle (M. tibialis cranialis), whereas two extensors (Mm. fibularis longus and gastrocnemius pars lateralis) show a complex pattern of derivation and loss. Previous biomechanical studies demonstrate that ossification increases the stiffness of tendons, making them stretch less under a given force. These structural and phylogenetic patterns are consistent with the view that hindlimb tendon ossification in woodcreepers is an adaptation to resist increased forces that act to extend the limb during vertical climbing. © 1993 Wiley-Liss, Inc.     

Homology of the palpebral and origin of supraorbital ossifications in ornithischian dinosaurs

Maidment, S.C.R. & Porro, L.B. 2010: Homology of the palpebral and origin of supraorbital ossifications in ornithischian dinosaurs. Lethaia , Vol. 43, pp. 95–111.
The palpebral is a small ossification that projects across the orbit in some ornithischian dinosaurs and its presence is considered a synapomorphy of the clade. By contrast, other ornithischians lack the palpebral but possess accessory ossifications, commonly termed supraorbitals, which form the dorsal margin of the orbit. The homology of the ornithischian palpebral to one or more of the supraorbitals is widely accepted in the literature, but this homology has never been explicitly tested and no hypotheses have been proposed regarding the function of the palpebral or why it was incorporated into the orbital margin. As homology is synonymous with synapomorphy, incorrect homology statements can lead to incorrect hypotheses of relationships being obtained during cladistic analysis. The primary and secondary homologies of the ornithischian palpebral and the anterior supraorbital of more derived members of the major ornithischian clades are tested and we demonstrate that these homology hypotheses can be accepted. Osteological correlates indicate that the palpebral supported a layer of connective tissue that roofed the orbit; ossification of this connective tissue resulted in the incorporation of the palpebral into the skull roof and gave rise to additional supraorbital elements, which are neomorphic ossifications. Large-scale structural changes in the ornithischian skull, including dermal ossifications associated with display or defence and the development of complex feeding mechanisms, may have led to the incorporation of the palpebral into the skull roof. □ Functional morphology , homology , Ornithischia , palpebral , supraorbital.     

The tarsus of erythrosuchid archosaurs, and implications for early diapsid phylogeny

The morphology of the erythrosuchid ankle joint is reassessed. Two specimens, recently thought to have been incorrectly referred to Erythrosuchus africanus , are shown without doubt to belong to this taxon. Furthermore, the morphology is essentially similar to that of other early archosaurs. The tarsus of Erythrosuchus is poorly ossified and consists of a calcaneum, astragalus, and two distal tarsals. The calcanea of Erythrosuchus, Vjushkovia triplicostata , and Shansisuchus shansisuchus are all similar in being dorsoventrally compressed, possessing a lateral tuber, and lacking a perforating foramen. The astragalus of V. triplicostata is currently unknown. The astragalus of Shansisuchus is apparently unique in form. The erythrosuchid pes is therefore more derived than has been recently proposed. The tarsal morphology of several other archosauromorph taxa is reviewed and many details are found to be at variance with the literature. The plesiomorphic condition for the Archosauromorpha consists of four distal tarsals and a proximal row of three elements; two of which articulate with the tibia. These proximal elements are interpreted as the astragalus, calcaneum, and a centrale, and the same pattern is retained in the earliest archosaurs. This reassessed tarsal morphology has implications for the homology of the centrale and reconstruction of early diapsid phylogeny.     

Postnatal skeletal ontogeny in Callisaurus draconoides and Uta stansburiana (Iguania: Phrynosomatidae).

The mineralization of the skeleton from hatching to near maximum size in two phrynosomatid lizards, Callisaurus draconoides and Uta stansburiana, is described in detail. Observed patterns in the appearance of epiphyseal secondary centers, ossification centers, apophyseal ossifications, and calcifications, the distribution of sesamoids, and the timing of fusions, are compared and contrasted with observations of other squamates available in the literature. Overall, Callisaurus and Uta exhibit an advanced state of ossification in the hatchling relative to other squamate neonates and share a similar sequence of braincase fusions and appearance of secondary centers. Preliminary observations suggest that patterns of postnatal skeletal development are highly conserved and independent of patterns of prenatal morphogenesis, and thus a potentially rich source of character data for systematic investigations.     

Ontogeny and phytogeny of the mesopodial skeleton in mosasauroid reptiles

Current phylogenics of mosasauroid reptiles are reviewed and a new phylogeny examining aigialosaur interrelationships presented. Patterns of mesopodial ossification and overall limb morphology are described for adult mosasauroids. Ossification sequences are mapped onto a phylogeny in order to assess the distribution of ontogenetic characters. Consistent and ordered distributions are found. Based on the phylogenetic distribution of ossification patterns, an overall mesopodial ossification sequence for mosasaurs is proposed. Carpal sequence: ulnare—distal carpal four (dc4)—intermedium—dc3—radiale or dc2—de1 or pisiform and dc5. Tarsal sequence: astragalus—distal tarsal four or calcaneum. Skeletal paedomorphosis is recognized as a dominant pattern in the evolution of mosasauroid limbs. Apomorphic characters of skeletal paedomorphosis, apparent in most taxa, reach extremes in tylosaurs. Arguments for the presence of a single proximal cartilage in the tarsus of mosasaurs are made. This cartilage is presumed to include ossification centres from which both the astragalus and calcaneum will ossify.     

Limb ossification patterns of the ichthyosaur Stenopterygius, and a discussion of the proximal tarsal row of ichthyosaurs and other neodiapsid reptiles

Limb ossification patterns for the Lower Jurassic (Toarcian) ichthyosaur, Stenopterygius , are described. It is found that limb ossification follows a continuous proximal to distal sequence from the propodial elements through to the terminal elements of 1st to 4th digit in the manus and the 1st to 3rd digit in the pes. The 5th manal and 4th pedal digit begin ossification later than more preaxial digits and also show evidence of proximal addition of elements near the distal mesopodial row in a manner consistent with delayed ossification of the 5th distal mesopodial in other diapsids. Ossification of manal elements in the Supernumerary 3–4 (S3-4) digit and the 5th digit appear interdependent; if one or the other is highly ossified, ossification of the other is retarded. The 1st pedal digit is considered to be lost in Stenopterygius and the 4th pedal digit is identified as the 5th digit. Delayed ossification of the mesopodium is not observed. The most preaxial proximal tarsal is identified as the centralc; the remaining proximal tarsals are the astragalus and calcaneum, and it is inferred that the astragalus and calcaneum ossified from within a single proximal cartilage.     

Postembryonic ontogeny of the spadefoot toad,Scaphiopus intermontanus (Anura: Pelobatidae): Skeletal morphology

Postembryonic skeletal ontogeny of the pelobatid frog Scaphiopus intermontanus is described based on a developmental series of cleared-and-stained, whole-mount specimens. The focus is on laboratory-reared individuals fed a herbivorous diet as larvae. Although there is variation in the timing of ossification of individual skeletal elements relative to developmental stages based on external morphological criteria, the sequence of skeletal development generally is conservative. Compared with its close relative, S. bombifrons, ossifications that occur during prometamorphosis tend to be slightly delayed in S. intermontanus; however, cranial bones that ossify during late metamorphic climax in S. intermontanus are delayed until postmetamorphosis in S. bombifrons. The differences in timing between the two species are consistent, however, with differences observed between two developmental series of S. intermontanus raised at two different temperatures. Noteworthy features of skeletal development in S. intermontanus include: 1) presence of palatine ossifications that form from independent centers of ossification and soon fuse with the postnarial portion of the vomers to form the compound vomeropalatine bones; 2) compound sphenethmoid that may arise from four or more endochondral centers of ossification and one dorsal, dermal center of ossification; and 3) presence of transverse processes and vestigal prezygapophyses on the first postsacral vertebra. The morphology of the larval orbitohyoideus and interhyoideus muscles is compared. The record of skeletal ontogeny and muscle morphology presented herein for the herbivorous larval morph can serve as a baseline for comparisons with the ontogeny of the carnivorous larval morph of Scaphiopus. J. Morphol. 238:179–244, 1998. © 1998 Wiley-Liss, Inc.     

Stance and gait in the hindlimb of a therocephalian mammal-like reptile

The ilium, femur, tibia, fibula, astragalus and calcaneum of the therocephalian therapsid Regisaurus jacobi Mendrez are described. Functional consideration of the bones and particularly the nature of the hip, knee and ankle joints indicate that this animal was capable of at least two distinct gaits, a primitive, sprawling type and an advanced upright type. The ankle joint had a moveable articulation between the astragalus and the calcaneum analogous to that of the crocodiles. The possibility of such a multi-gaited intermediate stage having occurred in the course of the evolution of the mammalian locomotory pattern is suggested.     

Studies on skeleton formation in reptiles. I. The postembryonic development of the skeleton in Cyrtodactylus pubisulcus (Reptilia: Gekkonidae)

The study of ossification during postembryonic development of the lizard Cyrtodactylus pubisulcus reveals consistent patterns in the skeleton of the body axis and of the limbs. The vertebral column shows a distinct antero-posterior gradient in ossification; the serial homology of sacral ribs and caudal transverse processes with dorsal ribs requires further scrutiny. The sequence of ossification of carpal and tarsal elements is constant, yet different from the pattern of chondrification as described in the literature. The homology of a separate 'intermedium' in the ossified lizard carpus requires further discussion. The development of the lizard astragalus is discussed in detail, as is the ossification of epiphyses in the limbs.     

A phylogenetic hot spot for evolutionary novelty in Middle American treefrogs

Among the various types of evolutionary changes in morphology, the origin of novel structures may be the most rare and intriguing. Here we show statistically that the origins of different novel structures may be correlated and phylogenetically clustered into "hot spots" of evolutionary novelty, in a case study involving skull elements in treefrogs. We reconstruct phylogenetic relationships within a clade of Middle American treefrogs based on data from 10 nuclear and four mitochondrial genes and then analyze morphological evolution across this tree. New cranial elements are rare among anurans and tetrapods in general, but three novel elements have evolved within this clade, with a 40% increase in the number of skull roof elements in some species. Two of these elements also evolved in a related clade of treefrogs, and these two novel elements may have each evolved repeatedly within one or both clades. The molecular phylogeny suggests striking homoplasy in cranial morphology and shows that parsimony and Bayesian analyses of the morphological data have produced misleading results with strong statistical support. The origins of the novel elements are associated with an overall increase in the ossification of dermal skull roof elements (suggesting peramorphosis) and with the evolution of a novel adaptive behavior. Our study may be the first to statistically document significant phylogenetic clustering and correlation in the origins of novel structures, and to demonstrate the strongly misleading effects of peramorphosis on phylogenetic analysis.     

Major transitions in the evolution of early land plants: a bryological perspective

Background Molecular phylogeny has resolved the liverworts as the earliest-divergent clade of land plants and mosses as the sister group to hornworts plus tracheophytes, with alternative topologies resolving the hornworts as sister to mosses plus tracheophytes less well supported. The tracheophytes plus fossil plants putatively lacking lignified vascular tissue form the polysporangiophyte clade. Scope This paper reviews phylogenetic, developmental, anatomical, genetic and paleontological data with the aim of reconstructing the succession of events that shaped major land plant lineages. Conclusions Fundamental land plant characters primarily evolved in the bryophyte grade, and hence the key to a better understanding of the early evolution of land plants is in bryophytes. The last common ancestor of land plants was probably a leafless axial gametophyte bearing simple unisporangiate sporophytes. Water-conducting tissue, if present, was restricted to the gametophyte and presumably consisted of perforate cells similar to those in the early-divergent bryophytes Haplomitrium and Takakia. Stomata were a sporophyte innovation with the possible ancestral functions of producing a transpiration-driven flow of water and solutes from the parental gametophyte and facilitating spore separation before release. Stomata in mosses, hornworts and polysporangiophytes are viewed as homologous, and hence these three lineages are collectively referred to as the 'stomatophytes'. An indeterminate sporophyte body (the sporophyte shoot) developing from an apical meristem was the key innovation in polysporangiophytes. Poikilohydry is the ancestral condition in land plants; homoiohydry evolved in the sporophyte of polysporangiophytes. Fungal symbiotic associations ancestral to modern arbuscular mycorrhizas evolved in the gametophytic generation before the separation of major present-living lineages. Hydroids are imperforate water-conducting cells specific to advanced mosses. Xylem vascular cells in polysporangiophytes arose either from perforate cells or de novo. Food-conducting cells were a very early innovation in land plant evolution. The inferences presented here await testing by molecular genetics.     

Development of the integument of Dasypus hybridus and Chaetophractus vellerosus,and asynchronous events with respect to the postcranium

The integument of extant armadillos (Xenarthra, Cingulata) is a unique organ in which complex glandular systems are associated with pilose follicles, dermal ossifications, and cornified scales. Up to date, papers have focused on neither comparative morphology of the skin (dorsal and ventral) nor chronology of the development of interspecific homolog structures. In order to clarify the way in which events occur during development of the integument structures, maturity of other tissues (e.g. skeletal tissues) should be considered. Therefore, we will be able to identify events that have been pre- or post-displaced during ontogenetic development. The aim of this paper is to describe in a developmental and comparative framework the integumentary system of neonates of Dasypus hybridus and Chaetophractus vellerosus. In order to understand the morphology of the different integumentary structures serial histological sections were prepared. Staining techniques included H–E, Masson Trichrome, PAS, orcein and reticulin. To study ossification of postcranial elements, the specimens were cleared and double-stained with alcian blue and alizarin red. Determinations of ossification centers and their progress were recorded through the early uptake of alizarin. The dorsal dermis of neonates from D. hybridus is clearly differentiated into a superficial and deep layer, as in fetuses of Dasypus novemcinctus. In C. vellerosus, however, these layers could not be identified. This suggests a less connective tissue differentiation in the latter species at this stage. Osteoderms in D. hybridus are well differentiated unlike C. vellerosus where no condensations of osteoprogenitory cells are observed. Conversely, pilose follicles and glandular tissues are less developed in D. hybridus. Regarding postcranial elements, ossification centers are less advanced in C. vellerosus than D. hybridus, this is particularly notorious for the vertebral column, sternal, and pelvic girdle elements. Asynchronies between neonates of both species observed on integumentary and postcranial skeletal tissues could match with specific adaptive strategies related to distribution in different environments, and/or different postnatal care.     

Skeletal development in the Chinese soft‐shelled turtle Pelodiscus sinensis (Testudines: Trionychidae)

We investigated the development of the whole skeleton of the soft‐shelled turtle Pelodiscus sinensis, with particular emphasis on the pattern and sequence of ossification. Ossification starts at late Tokita‐Kuratani stage (TK) 18 with the maxilla, followed by the dentary and prefrontal. The quadrate is the first endoskeletal ossification and appears at TK stage 22. All adult skull elements have started ossification by TK stage 25. Plastral bones are the first postcranial bones to ossify, whereas the nuchal is the first carapacial bone to ossify, appearing as two unstained anlagen. Extensive examination of ossification sequences among autopodial elements reveals much intraspecific variation. Patterns of ossification of cranial dermal elements are more variable than those of endochondral elements, and dermal elements ossify before endochondral ones. Differences in ossification sequences with Apalone spinifera include: in Pelodiscus sinensis the jugal develops relatively early and before the frontal, whereas it appears later in A. spinifera; the frontal appears shortly before the parietal in A. spinifera whereas in P. sinensis the parietal appears several stages before the frontal. Chelydrids exhibit an early development of the postorbital bone and the palatal elements as compared to trionychids. Integration of the onset of ossification data into an analysis of the sequence of skeletal ossification in cryptodirans using the event‐pairing and Parsimov methods reveals heterochronies, some of which reflect the hypothesized phylogeny considered taxa. A functional interpretation of heterochronies is speculative. In the chondrocranium there is no contact between the nasal capsules and planum supraseptale via the sphenethmoid commissurae. The pattern of chondrification of forelimb and hind limb elements is consistent with a primary axis and digital arch. There is no evidence of anterior condensations distal to the radius and tibia. A pattern of quasi‐ simultaneity is seen in the chondrogenesis of the forelimb and the hind limb. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Appendicular skeleton in Bachia bicolor (Squamata: Gymnophthalmidae): osteology,limb reduction and postnatal skeletal ontogeny

The osteology of the appendicular skeleton and its postnatal development are described in Bachia bicolor, a serpentiform lizard with reduced limbs. The pectoral girdle is well developed and the forelimb consists of a humerus, ulna, radius, five carpal elements (ulnare, radiale, distal carpals 4–3, centrale), four metacarpals (II, III, IV, V) and phalanges (phalangeal formula X‐2‐2‐2‐2). In the hindlimb, the femur is small and slender, and articulates distally with a series of ossified amorphous and extremely reduced elements that correspond to a fibula, tibia and proximal and distal tarsals 4 and 3. The pelvic girdle consists of ischium, pubis and ilium, but its two halves are widely separated; the ilium is the least reduced element. We describe the ossification and development during postnatal skeletal ontogeny, especially of epiphyseal secondary centres, ossifications of carpal elements, apophyseal ossifications and sesamoids. Compared to other squamates, B. bicolor shows an overall reduction in limb size, an absence of skeletal elements, a fusion of carpal elements, an early differentiation of apophyseal centres, and a low number of sesamoids and apophyseal centres. These observations suggest that the reductions are produced by heterochronic changes during postnatal development and probably during embryonic development; therefore the appendicular skeleton exhibits a pattern of paedomorphic features.     

Skeletal development in the African elephant and ossification timing in placental mammals

We provide here unique data on elephant skeletal ontogeny. We focus on the sequence of cranial and post-cranial ossification events during growth in the African elephant (Loxodonta africana). Previous analyses on ossification sequences in mammals have focused on monotremes, marsupials, boreoeutherian and xenarthran placentals. Here, we add data on ossification sequences in an afrotherian. We use two different methods to quantify sequence heterochrony: the sequence method and event-paring/Parsimov. Compared with other placentals, elephants show late ossifications of the basicranium, manual and pedal phalanges, and early ossifications of the ischium and metacarpals. Moreover, ossification in elephants starts very early and progresses rapidly. Specifically, the elephant exhibits the same percentage of bones showing an ossification centre at the end of the first third of its gestation period as the mouse and hamster have close to birth. Elephants show a number of features of their ossification patterns that differ from those of other placental mammals. The pattern of the initiation of the ossification evident in the African elephant underscores a possible correlation between the timing of ossification onset and gestation time throughout mammals.     

Intercentrum versus pleurocentrum growth in early tetrapods: A paleohistological approach

A variety of vertebral centrum morphologies have evolved within early tetrapods which range from multipartite centra consisting of intercentra and pleurocentra in stem‐tetrapods, temnospondyls, seymouriamorphs, and anthracosaurs up to monospondylous centra in lepospondyls. With the present study, we aim to determine the formation of both intercentrum and pleurocentrum and asked whether these can be homologized based on their bone histology. Both intercentra and pleurocentra ossified endochondrally and periosteal bone was subsequently deposited on the outer surface of the centra. Our observations indicate low histological variation between intercentrum and pleurocentrum in microstructural organization and growth which inhibits the determination of homologies. However, intercentrum and pleurocentrum development differs during ontogeny. As previously assumed, the intercentrum arises from ventrally located and initially paired ossification centers that fuse ventromedially to form the typical, crescentic, rhachitomous intercentrum. In contrast, presacral pleurocentra may be ancestrally represented by four ossification centers: a ventral and a dorsal pair. Subsequently, two divergent developmental patterns are observed: In stem‐tetrapods and temnospondyls, the pleurocentrum evolves from the two dorsally located ossification centers which may occasionally fuse to form a dorsal crescent. In some dvinosaurian temnospondyls, the pleurocentrum may even ossify to full rings. In comparison, the pleurocentrum of stem‐amniotes (anthracosaurs, chroniosuchids, seymouriamorphs, and lepospondyls) arises from the two ventrally located ossification centers whereby the ossification pattern is almost identical to that of temnospondyls but mirror‐inverted. Thus, the ring‐shaped pleurocentrum of Discosauriscus ossifies from ventral to dorsal. We also propose that the ossified portions of the intercentrum and pleurocentrum continued as cartilaginous rings or discs that surrounded the notochord in the living animals.     

New Study on Dental and Skeletal Features of the Cretaceous “Symmetrodontan” Mammal Zhangheotherium

A new partial skeleton of the Cretaceous “symmetrodontan” mammal Zhangheotherium quinquecuspedens from the Yixian Formation of Liaoning, China has shed light on the dental and skeletal features of this taxon. The new fossil is a juvenile individual of late growth stage, preserved with interesting features of the premolar replacement. This fossil also provides new information on the vertebral column, the pelvis, the hindlimb and pes. Zhangheotherium has a typical diphyodont replacement of its premolars that is characterized by an alternating pattern (p1 → p3 → p2). This alternating replacement of premolars is a derived condition shared by Dryolestes, Slaughteria, and some basal eutherians, and differs from the plesiomorphic sequential replacement of anterior postcanines in eutricondontans, in most multituberculates and in stem mammaliaforms. The calcaneus and astragalus in the ankle joint of Zhangheotherium lack superposition. This shows that the trechnotherian clade, of which Zhangheotherium is a basal taxon, has retained the primitive condition of mammaliaforms in which the astragalus is in juxtaposition with the calcaneus. Coupled with recent evidence from the earliest metatherians and eutherians, this suggests that the superposition of astragalus and calcaneus evolved in parallel in metatherians and eutherians.     

Phylogenetic evidence for a single long-lived clade of crustacean cyclic parthenogens and its implications for the evolution of sex

The short-term advantages of sexual reproduction are unclear, but the existence of groups that are capable of producing either meiotic or ameiotic eggs (cyclic parthenogenesis, CP) might indicate that short-term advantages to sex exist. Alternatively, CP might be an unstable transitory stage between asexuality and sex, or a phylogenetically favoured life cycle (i.e. clade selection). The extensive knowledge of breeding systems and population genetics in branchiopod crustaceans makes them a useful group to test phylogenetic predictions of these hypotheses. Several proponents favour the hypothesis that CP has evolved multiple times in five orders of branchiopod crustaceans. We inferred the first robust branchiopod phylogeny from nuclear rRNA sequence (SSU and LSU), morphology, and complex rRNA stem–loop structures to assess the phylogenetic distribution of cyclic parthenogenesis. The sequence-based, structural rRNA and total evidence phylogenies are concordant and suggest that cyclic parthenogenesis arose once in the branchiopods, that this clade is long-lived (at least since the Permian), and that it has radiated extensively into nearly every aqueous habitat without reverting to strict sexuality and only rarely transforming to strict asexuality. These results are consistent with the clade selection hypothesis but inconsistent with the predictions of the hypothesis that CP is a transitory stage that leads to strict sexual reproduction. The evidence also indicates that clade selection for CP is a viable alternative explanation for the maintenance of sex in CP life cycles.