Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals

Background Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development. Results An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification). Conclusions The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification

Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw.

The amniote jaw complex is a remarkable amalgamation of derivatives from distinct embryonic cell lineages. During development, the cells in these lineages experience concerted movements, migrations, and signaling interactions that take them from their initial origins to their final destinations and imbue their derivatives with aspects of form including their axial orientation, anatomical identity, size, and shape. Perturbations along the way can produce defects and disease, but also generate the variation necessary for jaw evolution and adaptation. We focus on molecular and cellular mechanisms that regulate form in the amniote jaw complex, and that enable structural and functional integration. Special emphasis is placed on the role of cranial neural crest mesenchyme (NCM) during the species-specific patterning of bone, cartilage, tendon, muscle, and other jaw tissues. We also address the effects of biomechanical forces during jaw development and discuss ways in which certain molecular and cellular responses add adaptive and evolutionary plasticity to jaw morphology. Overall, we highlight how variation in molecular and cellular programs can promote the phenomenal diversity and functional morphology achieved during amniote jaw evolution or lead to the range of jaw defects and disease that affect the human condition

Chondrogenic and ossification patterns and sequences in White’s skink Liopholis whitii (Scincidae, Reptilia)

The prenatal patterns and sequences of chondrogenesis and ossification are described for the skink Liopholis whitii; eight embryos and one adult specimen were examined. Cranial ossification begins in elements of the braincase and the palate, followed by areas of the lower jaw and the cranial roof. Ossification proceeds anteroposteriorly along the axial skeleton and from proximal to distal in the forelimbs and hind limbs. In the zeugopods, the ossification progresses from posterior to anterior, while there is also a strict postaxial order in the autopods with the predominance of digit III in the forelimb and digit IV in the hind limb. Ossification of the femur and tibia starts before the corresponding elements of the forelimb, but simultaneously with the onset in clavicles. Elements of the hind limb display advanced ossification with respect to their forelimb counterparts, with earlier uptake of Alizarin Red in the tarsals, metatarsals and phalanges. The preaxial area of the fused stragalocalcaneum-complex is first to begin ossification among the tarsals. The sequence of ossification is mostly conserved in the skeleton of squamates, as shown in a comparative analysis of heterochrony, but some shifts were found in cranial, vertebral and autopodial regions

Heterochronic shifts during early cranial neural crest cell migration in two ranid frogs

We describe the development of the cranial neural crest cell streams relative to embryonic events such as neural tube formation and somite appearance in two Eurasian frog species belonging to the Ranidae, Rana temporaria and Sylvirana nigrovittata, and demonstrate developmental heterochronies. The mandibular stream appeared well developed in R. temporaria at a time when the embryo was still spherical, the neural folds were elevated, and the neural plate was wide open, thus earlier than known from any frog species so far. The appearance of the second stream and its division into hyoid and branchial portions was clearly accelerated in R. temporaria relative to other embryonic events when compared to S. nigrovittata. For example, in R. temporaria, the hyoid and branchial portions of the cranial neural crest cell streams were separated before the neural folds had started to fuse, whereas in S. nigrovittata this event took place only after the neural folds had fused completely. Such ostentatious heterochronies related to the characters used herein have formerly only been reported from comparisons between species belonging to different higher taxa. Our results re-confirm that to understand the full dynamics of the evolution of development, studies need to implement comparative embryological approaches, and include phylogenetically relatively closely related taxa

Timing of ossification in duck, quail, and zebra finch: intraspecific variation, heterochronies, and life history evolution

Skeletogenic heterochronies have gained much attention in comparative developmental biology. The temporal appearance of mineralized individual bones in a species — the species ossification sequence — is an excellent marker in this kind of study. Several publications describe interspecific variation, but only very few detail intraspecific variation. In this study, we describe and analyze the temporal order of ossification of skeletal elements in the zebra finch, Taeniopygia guttata, the Japanese quail, Coturnix coturnix japonica, and the White Pekin duck, a domestic race of the mallard Anas platyrhynchos, and explore patterns of intraspecific variation in these events. The overall sequences were found to be conserved. In the duck, variability is present in the relative timing of ossification in the occipital, the basisphenoid and the otic regions of the skull and the phalanges in the postcranium. This variation appears generally in close temporal proximity. Comparison with previously published data shows differences in ossification sequence in the skull, the feet, and the pelvis in the duck, and especially the pelvis in the quail. This clearly documents variability among different breeds

Skeletal development and adult osteology of Hypsiboas pulchellus (Anura: Hylidae)

Abstract. Osteological and skeletal characters have long been proven to be particularly informative in taxonomic and systematic research. Furthermore, ossification sequences are assumed to be a potential tool to investigate developmental states and developmental modes of fossil and extant skeletal specimens. Herein, we provide a detailed account on adult osteology and skeletogenesis in the Montevideo treefrog, Hypsiboas pulchellus (Anura: Hylidae) based on evaluation of a series of cleared and stained specimens. A consensus sequence of ossification, i.e., the order of appearance of mineralized elements until early metamorphosis could be determined as (parasphenoid, presacral vertebrae I-VII, frontoparietal, exoccipital) – transverse processes of presacral vertebrae I-VIII – sacral vertebra – (humerus, radioulna, ilium, femur, tibiofibula, scapula) – (cleithrum, clavicle, coracoids, metacarpals, tarsals, metatarsals, phalanges, hypochord) – (prootic, angulosplenial, dentary, maxilla, premaxilla, squamosal). Comparing the state of mineralized elements in individual specimens, a number of skeletal elements, including the exoccipital, frontoparietal, parasphenoid and prootic, as well as elements of the shoulder and pelvic girdles, and the phalanges, were found to vary intraspecifically regarding the relative time of their ossification within the ossification sequence

Transcriptional heterochrony in talpid mole autopods

BACKGROUND: Talpid moles show many specializations in their adult skeleton linked to fossoriality, including enlarged hands when compared to the feet. Heterochrony in developmental mechanisms is hypothesized to account for morphological evolution in skeletal elements. METHODS: The temporal and spatial distribution of SOX9 expression, which is an early marker of chondrification, is analyzed in autopods of the fossorial Iberian mole Talpa occidentalis, as well as in shrew (Cryptotis parva) and mouse (Mus musculus) for comparison. RESULTS AND DISCUSSION: SOX9 expression is advanced in the forelimb compared to the hind limb in the talpid mole. In contrast, in the shrew and the mouse, which do not show fossorial specializations in their autopods, it is synchronous. We provide evidence that transcriptional heterochrony affects the development of talpid autopods, an example of developmental penetrance. We discuss our data in the light of earlier reported pattern heterochrony and later morphological variation in talpid limbs. CONCLUSION: Transcriptional heterochrony in SOX9 expression is found in talpid autopods, which is likely to account for pattern heterochrony in chondral limb development as well as size variation in adult fore- and hind limbs