Paedomorphosis and skull structure in Malagasy chamaeleons (Reptilia: Chamaeleoninae)

The phylogenetic analysis of skull characteristics, along with data derived from lung and hemipenial morphology, does not support monophyly of the predominantly terrestrial chamaeleons, Brookesiinae ( Brookesia plus Rhampholeon ), as sister-taxon of a monophyletic clade of arboreal chamaeleons, the Chamaeleoninae. Instead, the phylogenetic interrelationships of chamaeleonine lizards are ( Brookesia ("Rhampholeon" (Bradypodion, Chamaeleo) ). The monophyly of the genus Rhampholeon is not demonstrated. The arboreal chamaeleons form a monophyletic group comprising two genera, Bradypodion and Chamaeleo. Bradypodion may be placed as sister-group of the genus Chamaeleo , but its phyletic position and monophyly cannot at present be corroborated.
This study documents that there is a high degree of intraspecific variability in skull characters which may be due to paedomorphic reduction in the skull, especially of small species. Characters affected by a variable degree of ossification include the separation of a prefrontal fontanelle, the contact of the squamosal with the parietal, the size and position of the fenestra vestibuli, the degree of ossification in the basicranial rim of the fenestra, the extent of ossification of the pterygoid wing, and the shape of the skull roof as indicated by the bones forming the dorsal margin of the orbit. The closure of the lateral aperture of the occipital recess might indicate that miniaturization, and concomitant paedomorphosis, may have played a role in the initial phases of chamaeleonine phylogeny.     

Development of the Osteocranium in Natrix natrix (Serpentes,Colubridae) Embryogenesis II: Development of the jaws,palatal complex and associated bones

Snakes differ from the other vertebrates with their hyperkinetic skull. To establish the developmental features of the skull bones, involved in prey capture and ingestion, the Grass snake Natrix natrix (Serpentes, Colubridae) embryos are studied at all the successive stages of embryogenesis. Thirty-five N. natrix embryos are examined. Twenty embryos are studied with histological methods; fifteen embryos are cleared and double-stained with alizarin red and alcian blue. The sequence of appearance and formation of the upper and lower jaw bones, palatal complex and associated bones is described in accordance with the table of developmental stages. New features in the ossification mode of some bones are revealed: each bone, namely, the vomer, septomaxilla and maxilla, is formed from three separate ossification centres. Three ossification centres in the maxilla, two ossification centres in the bodies of the septomaxilla and vomer, as well as the unknown additional ossification centre in the vomer had not been previously described in snake embryos. The new data can be used in further comparative research on the reptile skull development and vertebrate phylogeny.     

The cranial development of Elaphe obsoleta (Ophidia,colubridae)

The kinetic skull of snakes is a highly specialized structure that has allowed these limbless organisms to exploit a wide variety of habitats. Here we analyze the development of the cranium in the colubrid snake Elaphe obsoleta quadrivittata based on two sets of embryos raised under controlled conditions and preserved at regular intervals during embryogenesis. Emphasis is on the interactions between dermal and endochondral ossification in the basicranium and in the posterior orbitotemporal region. In Elaphe, the laterosphenoid initially develops as an ascending process of the basal plate and is a combination of membrane and cartilage bone. The maxilla shows a peculiar pattern of differentiation from several centers of ossification.     

The development of the skull in Acrochordus granulatus (Schneider) (Reptilia: Serpentes), with special consideration of the otico-occipital complex

The skull of Acrochordus has been characterized by the absence of a crista circumfenestralis (a synapomorphy shared by all snakes), and by the absence of a recessus scalae tympani that in other squamates forms by subdivision of the embryonic metotic fissure. These traits have variably been identified as either plesiomorphic or paedomorphic. The study of the development of the osteocranium in a series of cleared and stained embryos of Acrochordus shows a close correspondence to the development of the skull in other snakes. The exception is the formation of the postorbital from two ossification centers. The significance of this observation, which might suggest the embryonic fusion of a postfrontal with a postorbital, remains enigmatic, as it is based on one side only of the skull of a single specimen. By contrast, a rudimentary and modified crista circumfenestralis can be identified in the skull of Acrochordus. Furthermore, absence of a recessus scalae tympani is not due to an undivided fissura metotica, but results from the obliteration of the anterior part of the metotic fissure instead. With respect to this character, Acrochordus is neither plesiomorphic, nor paedomorphic, but autapomorphic. This interpretation of the skull of Acrochordus is compatible with the sister-group relationships this genus shares with colubroid snakes.     

Comparative ossification and development of the skull in palaeognathous birds (Aves: Palaeognathae)

Ratites and tinamous are a morphologically diverse group of flightless and weakly flighted birds. As one of the most basal clades of extant birds, they are frequently used as an outgroup for studies discussing character evolution within other avian orders. Their skeletal development is not well known in spite of their important phylogenetic position, and studies have historically been plagued with small sample sizes and limited anatomical and temporal scope. Here, I describe the ossification of the skull in the emu (Dromaius novaehollandiae), ostrich (Struthio camelus), greater rhea (Rhea americana), and elegant crested‐tinamou (Eudromia elegans). Skeletal development is remarkably consistent within palaeognaths, in spite of large differences in absolute size and incubation period. Adult morphology appears to play a role in interordinal differences in the sequence and timing of ossification of certain bones. Neither the timing of cranial ossification events relative to stage nor the sequence of ossification events provides any evidence in support of a paedomorphic origin of the palaeognathous palate. This study provides an important first look at the timing and sequence of skull development in palaeognathous birds, providing data that can be compared to better‐studied avian systems in order to polarize ontogenetic characters. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 184–200.     

Changes of Skull Proportions in Ontogeny of Barbus canis from Lake Kinneret and of the Lake Tana large-mouthed barbs, Barbus intermedius Complex

Skull proportions of Barbus canis individuals drastically change during their life. Yearlings have skull proportions characteristic for barbs of the NEC phenetic group (sensu Mina et al. 2001 Environ. Biol. Fish. 61: 242–252), but with age become similar to those of the Lake Tana large-mouthed morphotypes which acquire their specific features at 3–7 years old while at earlier ages they have skull proportions of a NEC form identified as 'intermedius' sensu Nagelkerke et al. (1994 Environ. Biol. Fish. 39: 1–21). The large-mouthed Lake Tana barbs originated from an ancestral NEC form through peramorphosis, but in relation to B. canis they are paedomorphic in skull proportions. B. canis supposedly originated from a NEC form as a consequence of an adaptive radiation that took place in western Asia.     

Developmental plasticity of limb bone microstructural organization in Apateon: histological evidence of paedomorphic conditions in branchiosaurs

SUMMARY Apateon, a key genus among Branchiosauridae from the Carboniferous—Permian of Europe, is often considered closely related to salamanders on the basis of developmental similarities, anatomical features, and life history. The current work deals with recognition of heterochronies among three “time‐averaged populations” of Apateon based on inference from histological features already studied in extant urodeles. Our study is performed on the long bones of 22 specimens of Apateon pedestris and Apateon caducus. Histological observations show that diaphyseal and epiphyseal ossification patterns of Apateon are similar to those of urodeles. From skeletochronological analysis, the identification of the age of sexual maturity allows us to discriminate juveniles from adults and to confirm the previous hypothesis of a paedomorphic condition based on anatomical data among these species. The current study also suggests a paedomorphic condition of each “population” at the histological level. This heterochrony may have been linked to peculiar ecological conditions such as hypoxic and fresh water environment. Functional reasons may also be invoked to explain differences of ossification between fore‐ and hindlimbs of the “populations” from Odernheim and Niederkirchen because paleoecological conditions are very different from one locality to another. This study illustrates the role that the acquisition of heterochronic features plays at the microevolutionary scale.     

A New Snake Skull from the Paleocene of Bolivia Sheds Light on the Evolution of Macrostomatans

Macrostomatan snakes, one of the most diverse extant clades of squamates, display an impressive arsenal of cranial features to consume a vast array of preys. In the absence of indisputable fossil representatives of this clade with well-preserved skulls, the mode and timing of these extraordinary morphological novelties remain obscure. Here, we report the discovery of Kataria anisodonta n. gen. n. sp., a macrostomatan snake recovered in the Early Palaeocene locality of Tiupampa, Bolivia. The holotype consists of a partial, minute skull that exhibits a combination of booid and caenophidian characters, being the presence of an anisodont dentition and diastema in the maxilla the most distinctive trait. Phylogenetic analysis places Kataria basal to the Caenophidia+Tropidophiidae, and represents along with bolyeriids a distinctive clade of derived macrostomatans. The discovery of Kataria highlights the morphological diversity in the maxilla among derived macrostomatans, demonstrating the relevance of maxillary transformations in the evolution of this clade. Kataria represents the oldest macrostomatan skull recovered, revealing that the diversification of macrostomatans was well under way in early Tertiary times. This record also reinforces the importance of Gondwanan territories in the history of snakes, not only in the origin of the entire group but also in the evolution of ingroup clades.     

Variation and timing of the cranial ossification sequence of the oriental fire-bellied toad,Bombina orientalis (Amphibia,Discoglossidae)

The sequence of appearance of the 17 different skull bones in the oriental fire-bellied toad, Bombina orientalis, is described. Data are based primarily on samples of ten or 11 laboratory-reared specimens of each of 11 Gosner developmental stages (36–46) representing middle through late metamorphosis. Ossification commences as early as stage 37 (hind limb with all five toes distinct), but the full complement of adult bones is not attained until stage 46 (metamorphosis complete). Number of bones present at intermediate stages is poorly correlated with external morphology. As many as four Gosner developmental stages elapse before a given bone is present in all specimens following the stage at which it may first appear. The modal ossification sequence is frontoparietal, exoccipital, parasphenoid, septomaxilla, premaxilla, vomer, nasal, maxilla, angulosplenial, dentary, squamosal, quadratojugal, pterygoid, prootic, interfrontal, sphenethmoid, and mentomeckelian. Most specimens are consistent with this sequence, despite the poor correlation between cranial ossification and external development as assayed by Gosner stage. The timing of cranial ossification in Bombina orientalis differs in many respects from that described for two other, distantly related anurans, the leopard frog (Rana pipiens) and the western toad (Bufo boreas). These include the total number and sequence of appearance of bones, and the timing of ossification relative to the development of external morphology. Interspecific variation may reflect differences in the timing of the tissue interactions known to underlie skeletal differentiation and evolution.     

Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles

Snakes possess a derived anatomy, characterized by limb reduction and reorganization of the skull and internal organs. To understand the origin of snakes from an ontogenetic point of view, we conducted comprehensive investigations on the timing of skeletal elements, based on published and new data, and reconstructed the evolution of the ossification sequence among squamates. We included for the first time Varanus, a critical taxon in phylogenetic context. There is comprehensive delay in the onset of ossification of most skeletal elements in snakes when compared to reference developmental events through evolution. We hypothesize that progressing deceleration accompanied limb reduction and reorganization of the snake skull. Molecular and morphological studies have suggested close relationship of snakes to either amphisbaenians, scincids, geckos, iguanids, or varanids. Likewise, alternative hypotheses on habitat for stem snakes have been postulated. Our comprehensive heterochrony analyses detected developmental shifts in ossification for each hypothesis of snake origin. Moreover, we show that reconstruction of ancestral developmental sequences is a valuable tool to understand ontogenetic mechanisms associated with major evolutionary changes and test homology hypotheses. The “supratemporal” of snakes could be homolog to squamosal of other squamates, which starts ossification early to become relatively large in snakes.     

Ontogeny of the maxillary barbel muscles in Clarias gariepinus (Siluroidei: Clariidae), with some notes on the palatine-maxillary mechanism

Siluroids are characterized by the presence of a palatine-maxillary mechanism, which enables a controlled mobility of the maxillary barbels. In Clarias gariepinus , the ontogeny of this mechanism is studied and described as well as those muscles related to the maxillary barbel. Two muscles are distinguished: (1) retractor tentaculi , connecting the maxilla to the suspensorium, and (2) extensor tentaculi , running from the ventro-lateral face of the skull to the posterior half of the palatine. These typical catfish muscles are derived from muscles that are present in generalized teleost fishes. The retractor muscle is believed to be derived from the A₃ muscle of the adductor mandibulae complex. The extensor muscle is formed from the anterior fibres of the adductor arcus palatini. The palatine is rod-like in C. gariepinus and articulates with the orbitonasal lamina in larval specimens and with its ossification, the lateral ethmoid, in juvenile and adult specimens. The articulation occurs via a long cartilaginous strip on the dorsal face of the autopalatine, thereby enabling both a rotation and a restricted sliding.     

Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander,Bolitoglossa occidentalis (Amphibia: Plethodontidae)

Bolitoglossa occidentalis, a lowland salamander of Mexico and Guatemala, has a highly derived morphology. The features that are derived with respect to the condition in generalized members of the genus include the following: (1) small body size; (2) short tail; (3) fully webbed hands and feet; (4) reduction and loss of certain phalangeal elements; (5) fusion of carpals and tarsals; (6) absence of prefrontal bones; and (7) reduced skull ossification. The ontogeny of this species was analyzed quantitatively and compared with the patterns of growth and differentiation encountered in two morphologically generalized members of the genus, B. rostrata and B. subpalmata. Most of the derived features can be explained by invoking a single heterochronic process: truncation of development at a small size (most likely the product of early maturation). Therefore, B. occidentalis is a paedomorphic species whose morphology has been attained through the process of progenesis. This result supports Alberch's ('80a) prediction, based on functional analysis, that the principle adaptation to arboreality in B. occidentalis is small size; other derived morphological features are associated with the organism's truncated development and may have no adaptive significance. However, patterns of dissociation are found within this overall progenetic process. Some of these include the following: (1) accelerated growth rates of the metatarsals and first phalanges, and retarded growth rates of the second and third phalangeal elements; (2) dissociation between rates of ossification of the skull and the autopodial elements; and (3) dissociation between the timing of termination of the process of shape change during the ontogeny of the foot (the product of differential growth between digital and interdigital areas) and termination of growth in overall foot size (foot surface area). This later result illustrates the independence of morphogenetic phenomena (shape change) from processes of growth (size increase).     

The phylogenetic position of an undescribed paedomorphic clupeiform taxon: mitogenomic evidence

Molecular characters may offer a useful alternative to confidently estimate the phylogenetic position of paedomorphic taxa otherwise difficult to place based on morphology because of the reduction or absence of characters in their larvae-like adult stage. Here, we sequenced the complete mitogenome of a remarkable undescribed marine paedomorphic clupeiform fish to gain insight into its phylogenetic position. Of a length of 17,507 bp, this mitogenome exhibits a unique gene order within the Teleostei because of the inversion of the contiguous tRNA^Gln and tRNA^Ile within the IQM region and the presence of a putative second control region inserted between these tRNAs. Mitogenomic data from 27 clupeiform species and 22 non-clupeiform species were subjected to partitioned maximum likelihood and Bayesian analyses. All resultant phylogenetic trees strongly supported the placement of this undescribed taxon within the order Clupeiformes, suborder Clupeoidei, and the family Clupeidae, as the sister group of the tribe Spratelloidini (Jenkinsia + Spratelloides) of the subfamily Dussumieriinae. Together, they form a monophyletic group with Chirocentrus and, possibly, Etrumeus. Despite its overall resemblance to Sundasalanx, this undescribed taxa (Clupeidae gen. et sp. indet.) is not closely related to that genus and represents an independent paedomorphic lineage within the Clupeoidei. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The function of the intramaxillary joint in the Round Island boa, Casarea dussumieri

The bolyeriid snakes Casarea dussumieri and Bolyeria multocarinata are unique among vertebrates in possessing an intramaxillary joint that separates the maxilla into anterior and posterior segments. In contrast to previous studies, which suggest that this joint permits enhanced elevation of the anterior maxillary teeth, our films of live Casarea show that the snout and anterior maxillary teeth are actively depressed 15° 20° below rest position through bilateral retraction of the palatomaxillary arches. Patterns of bone movement in living Casarea support the hypothesis that a caudally directed force is transmitted to the snout via the medial bones of the palatomaxillary arch, suggesting functional affinities between Casarea and higher henophidians.
The intramaxillary joint, in conjunction with the curvature of the mandibles, allows the jaws of Casarea to encircle hard, cylindrical prey held transversely in the mouth. Because the Mauritian terrestrial vertebrate fauna lacks mammals and is dominated by skinks and geckos, which Casarea is known to consume, we suggest that the intramaxillary joint functions in a manner analogous to that achieved by quite different maxillary modifications in colubrid scincivores. Although the origin of the bolyeriid intramaxillary joint remains unclear, its structural refinement and evolutionary stability may be due to selection pressures arising from limited prey diversity.     

Tissue origins and interactions in the mammalian skull vault.

During mammalian evolution, expansion of the cerebral hemispheres was accompanied by expansion of the frontal and parietal bones of the skull vault and deployment of the coronal (fronto-parietal) and sagittal (parietal-parietal) sutures as major growth centres. Using a transgenic mouse with a permanent neural crest cell lineage marker, Wnt1-Cre/R26R, we show that both sutures are formed at a neural crest-mesoderm interface: the frontal bones are neural crest-derived and the parietal bones mesodermal, with a tongue of neural crest between the two parietal bones. By detailed analysis of neural crest migration pathways using X-gal staining, and mesodermal tracing by DiI labelling, we show that the neural crest-mesodermal tissue juxtaposition that later forms the coronal suture is established at E9.5 as the caudal boundary of the frontonasal mesenchyme. As the cerebral hemispheres expand, they extend caudally, passing beneath the neural crest-mesodermal interface within the dermis, carrying with them a layer of neural crest cells that forms their meningeal covering. Exposure of embryos to retinoic acid at E10.0 reduces this meningeal neural crest and inhibits parietal ossification, suggesting that intramembranous ossification of this mesodermal bone requires interaction with neural crest-derived meninges, whereas ossification of the neural crest-derived frontal bone is autonomous. These observations provide new perspectives on skull evolution and on human genetic abnormalities of skull growth and ossification.     

Late embryos and bony skull development in Bothropoides jararaca (Serpentes,Viperidae)

In recent years, developmental anatomy received increasing interest as a potential new source for phylogenetic research. For skeletal development, studies mainly rely on the first appearance of ossification centers. However, informative events occur during the whole course of skeletogenesis; interactions between external and internal development occur and morphometric changes take place – all of which present potential sources for phylogenetic analyses. Therefore, the Standard Event System (SES) was used to traceably describe the external development of the snake species Bothropoides jararaca and external measurements were analyzed. We then applied micro-computed tomography (μCT), clearing and double-staining, and 2D and 3D morphometric methods to describe, illustrate, and analyze the development of the head in great detail. We found a 3D flattening of the skull during ontogeny, a pattern that is not reflected in external development. This may be explained by a different relationship of skeletogenesis and external characters to the developing jaw musculature or simply by the different type of data. Clearing and double-staining and μCT-scanning revealed a broadly similar sequence in the onset of ossification. Minute differences may be due to the treatment of embryos. Bones of the dermatocranium are among the first to ossify and the development of the calcified endolymph may reflect its function as a calcium source during development. The value of phylogenetic observations using the sequence of first ossifications is critically discussed. The related heterochronic changes are interpreted to contribute at least to the very first phase of divagating skull formation among taxa.     

Pecularities of bony skeleton development in Asian clawed salamanders (Onychodactylus, Hynobiidae) related to embryonization

We studied skull, vertebral column, and limb skeleton development in Japanese clawed salamander Onychodactylus japonicus (Hynobiidae). The study is based on the ontogenetic series of embryos and larvae obtained from wild-captured adults by artificial induction of breeding using hormonal stimulation. The first stages of the skeleton formation in O. japonicus are shifted to the late embryonic period and hatching larvae already possess a well-ossified vertebral column, large number of skull ossifications and show signs of ossification in the forelimb skeleton. Compared to the primitive pattern of the skeleton development typical for other hynobiid salamanders, O. japonicus shows a number of heterochronies related to embryonization. In particular, this species is characterized by an earlier ossification of the vertebral column compared to that of the skull and by the delayed development and early reduction of the coronoid. Our results, along with the previously reported data on the skeleton development in the Fischer’s clawed salamander O. fischeri (Smirnov and Vassilieva, 2002), indicate that the genus Onychodactylus is characterized by the loss or reduction of several skeletal features typically found at early larval stages in other Hynobiidae species. In particular, provisional bones (especially the coronoid) and their dentition are underdeveloped. In addition, it is corroborated that the first tooth generation is absent in Onychodactylus, whereas such monocuspid nonpedicellate tooth generation normally develops at the early larval stages of other caudate amphibians. Since similar patterns of skeleton ontogeny are observed in other caudate groups with different extent of embryonization, it is proposed that, in different lineages of Urodela, the evolution of ontogeny followed similar pathways and was accompanied by the same changes in skeletogenesis.