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.

BackgroundHere 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.ResultsAn 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).ConclusionsThe 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.

Most anurans have a biphasic life cycle, which includes metamorphosis from a tadpole stage to an adult frog. This process involves extensive transformations of the cranial skeleton, which have been of long-standing interest with respect to anuran skeletal evolution and taxonomy. In this study, large-scale patterns of anuran skeletal ossification are assessed by collecting the most comprehensive data set on anuran cranial ossification to date from the literature, including data for 45 anuran and one caudate outgroup species. Ossification sequences were translated into event-pair matrices for explorative phylogenetic analysis and phylogenetically informed parsimony search for heterochrony using the Parsimov algorithm. Rank variability of single bones across species was also analysed. Little phylogenetic signal was retrieved from a parsimony-based phylogenetic analysis of event-pairs, and only a few species that are generally agreed to be closely related are placed close to each other (e.g. some Pipidae and Costata). Parsimov analysis revealed some clade-specific heterochrony in anuran clades of varying inclusiveness. Our results show that relating heterochronic changes in anuran cranial ontogeny to parameters such as direct development or miniaturization is problematic because of the high evolvability of cranial ossification sequences. Rank variation analysis suggests that anuran cranial bones are highly variable in their sequence positioning, possibly because tadpole and adult cranial morphology do not co-evolve. Elements which are lost in some species ossify at the end of the sequence, providing evidence for the notion that failure of anuran cranial elements to ossify is due to processes of paedomorphosis.

Data documenting skeletal development in rodents, the most species-rich 'order' of mammals, are at present restricted to a few model species, a shortcoming that hinders exploration of the morphological and ecological diversification of the group. In this study we provide the most comprehensive sampling of rodent ossification sequences to date, with the aim of exploring whether heterochrony is ubiquitous in rodent evolution at the onset of skeletal formation. The onset of ossification in 17 cranial elements and 24 postcranial elements was examined for eight muroid and caviomorph rodent species. New data are provided for two non-model species. For one of these, the African striped mouse, Rhabdomys pumilio, sampling was extended by studying 53 autopodial elements and examining intraspecific variation. The Parsimov method of studying sequence heterochrony was used to explore the role that changes in developmental timing play in early skeletal formation. Few heterochronies were found to diagnose the muroid and caviomorph clades, suggesting conserved patterning in skeletal development. Mechanisms leading to the generation of the wide range of morphological diversity encapsulated within Rodentia may be restricted to later periods in development than those studied in this work. Documentation of skeletogenesis in Rhabdomys indicates that intraspecifc variation in ossification sequence pattern is present, though not extensive. Our study suggests that sequence heterochrony is neither pivotal nor prevalent during early skeletal formation in rodents.

Mitgutsch, C., Piekarski, N., Olsson, L. and Haas, A. 2008. Heterochronic shifts during early cranial neural crest cell migration in two ranid frogs. -Acta Zoologica (Stockholm) 89 : 69-78We 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.