The role of embryo movement in the development of the furcula

The pectoral girdle is a complex structure which varies in its morphology between species. A major component in birds is the furcula, which can be considered equivalent to a fusion of the paired clavicles found in many mammals, and the single interclavicle found in many reptiles. These elements are a remnant of the dermal skeleton and the only intramembranous bones in the trunk. Postnatally, the furcula plays important mechanical roles by stabilising the shoulder joint and acting as a mechanical spring during flight. In line with its mechanical role, previous studies indicate that, unlike many other intramembranous bones, furcula growth during development can be influenced by mechanical stimuli. This study investigated the response of individual aspects of furcula growth to both embryo immobilisation and hypermotility in the embryonic chicken. The impact of altered incubation temperature, which influences embryo motility, on crocodilian interclavicle development was also explored. We employed whole‐mount bone and cartilage staining and 3D imaging by microCT to quantify the impact of rigid paralysis, flaccid paralysis and hypermobility on furcula growth in the chicken, and 3D microCT imaging to quantify the impact of reduced temperature (32–28 °C) and motility on interclavicle growth in the crocodile. This revealed that the growth rates of the clavicular and interclavicular components of the furcula differ during normal development. Total furcula area was reduced by total unloading produced by flaccid paralysis, but not by rigid paralysis which maintains static loading of embryonic bones. This suggests that dynamic loading, which is required for postnatal bone adaptation, is not a requirement for prenatal furcula growth. Embryo hypermotility also had no impact on furcula area or arm length. Furcula 3D shape did, however, differ between groups; this was marked in the interclavicular component of the furcula, the hypocleideum. Hypocleideum length was reduced by both methods of immobilisation, and interclavicle area was reduced in crocodile embryos incubated at 28 °C, which are less motile than embryos incubated at 32 °C. These data suggest that the clavicular and interclavicle components of the avian furcula respond differently to alterations in embryo movement, with the interclavicle requiring both the static and dynamic components of movement‐related loading for normal growth, while static loading preserved most aspects of clavicle growth. Our data suggest that embryo movement, and the mechanical loading this produces, is important in shaping these structures during development to suit their postnatal mechanical roles

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

Modularity of the rodent mandible: Integrating bones, muscles, and teeth

Several models explain how a complex integrated system like the rodent mandible can arise from multiple developmental modules. The models propose various integrating mechanisms, including epigenetic effects of muscles on bones. We test five for their ability to predict correlations found in the individual (symmetric) and fluctuating asymmetric (FA) components of shape variation. We also use exploratory methods to discern patterns unanticipated by any model. Two models fit observed correlation matrices from both components: (1) parts originating in same mesenchymal condensation are integrated, (2) parts developmentally dependent on the same muscle form an integrated complex as do those dependent on teeth. Another fits the correlations observed in FA: each muscle insertion site is an integrated unit. However, no model fits well, and none predicts the complex structure found in the exploratory analyses, best described as a reticulated network. Furthermore, no model predicts the correlation between proximal parts of the condyloid and coronoid, which can exceed the correlations between proximal and distal parts of the same process. Additionally, no model predicts the correlation between molar alveolus and ramus and/or angular process, one of the highest correlations found in the FA component. That correlation contradicts the basic premise of all five developmental models, yet it should be anticipated from the epigenetic effects of mastication, possibly the primary morphogenetic process integrating the jaw coupling forces generated by muscle contraction with those experienced at teeth.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/73767/1/j.1525-142X.2008.00290.x.pd

Visual Laterality of Calf–Mother Interactions in Wild Whales

Behavioral laterality is known for a variety of vertebrate and invertebrate animals. Laterality in social interactions has been described for a wide range of species including humans. Although evidence and theoretical predictions indicate that in social species the degree of population level laterality is greater than in solitary ones, the origin of these unilateral biases is not fully understood. It is especially poorly studied in the wild animals. Little is known about the role, which laterality in social interactions plays in natural populations. A number of brain characteristics make cetaceans most suitable for investigation of lateralization in social contacts.) in the greatest breeding aggregation in the White Sea. Here we show that young calves (in 29 individually identified and in over a hundred of individually not recognized mother-calf pairs) swim and rest significantly longer on a mother's right side. Further observations along with the data from other cetaceans indicate that found laterality is a result of the calves' preference to observe their mothers with the left eye, i.e., to analyze the information on a socially significant object in the right brain hemisphere.Data from our and previous work on cetacean laterality suggest that basic brain lateralizations are expressed in the same way in cetaceans and other vertebrates. While the information on social partners and novel objects is analyzed in the right brain hemisphere, the control of feeding behavior is performed by the left brain hemisphere. Continuous unilateral visual contacts of calves to mothers with the left eye may influence social development of the young by activation of the contralateral (right) brain hemisphere, indicating a possible mechanism on how behavioral lateralization may influence species life and welfare. This hypothesis is supported by evidence from other vertebrates

Mechanical Influences on Morphogenesis of the Knee Joint Revealed through Morphological, Molecular and Computational Analysis of Immobilised Embryos

Very little is known about the regulation of morphogenesis in synovial joints. Mechanical forces generated from muscle contractions are required for normal development of several aspects of normal skeletogenesis. Here we show that biophysical stimuli generated by muscle contractions impact multiple events during chick knee joint morphogenesis influencing differential growth of the skeletal rudiment epiphyses and patterning of the emerging tissues in the joint interzone. Immobilisation of chick embryos was achieved through treatment with the neuromuscular blocking agent Decamethonium Bromide. The effects on development of the knee joint were examined using a combination of computational modelling to predict alterations in biophysical stimuli, detailed morphometric analysis of 3D digital representations, cell proliferation assays and in situ hybridisation to examine the expression of a selected panel of genes known to regulate joint development. This work revealed the precise changes to shape, particularly in the distal femur, that occur in an altered mechanical environment, corresponding to predicted changes in the spatial and dynamic patterns of mechanical stimuli and region specific changes in cell proliferation rates. In addition, we show altered patterning of the emerging tissues of the joint interzone with the loss of clearly defined and organised cell territories revealed by loss of characteristic interzone gene expression and abnormal expression of cartilage markers. This work shows that local dynamic patterns of biophysical stimuli generated from muscle contractions in the embryo act as a source of positional information guiding patterning and morphogenesis of the developing knee joint

Evolution of the patellar sesamoid bone in mammals

The patella is a sesamoid bone located in the major extensor tendon of the knee joint, in the hindlimb of many tetrapods. Although numerous aspects of knee morphology are ancient and conserved among most tetrapods, the evolutionary occurrence of an ossified patella is highly variable. Among extant (crown clade) groups it is found in most birds, most lizards, the monotreme mammals and almost all placental mammals, but it is absent in most marsupial mammals as well as many reptiles. Here, we integrate data from the literature and first-hand studies of fossil and recent skeletal remains to reconstruct the evolution of the mammalian patella. We infer that bony patellae most likely evolved between four and six times in crown group Mammalia: in monotremes, in the extinct multituberculates, in one or more stem-mammal genera outside of therian or eutherian mammals and up to three times in therian mammals. Furthermore, an ossified patella was lost several times in mammals, not including those with absent hindlimbs: once or more in marsupials (with some re-acquisition) and at least once in bats. Our inferences about patellar evolution in mammals are reciprocally informed by the existence of several human genetic conditions in which the patella is either absent or severely reduced. Clearly, development of the patella is under close genomic control, although its responsiveness to its mechanical environment is also important (and perhaps variable among taxa). Where a bony patella is present it plays an important role in hindlimb function, especially in resisting gravity by providing an enhanced lever system for the knee joint. Yet the evolutionary origins, persistence and modifications of a patella in diverse groups with widely varying habits and habitats—from digging to running to aquatic, small or large body sizes, bipeds or quadrupeds—remain complex and perplexing, impeding a conclusive synthesis of form, function, development and genetics across mammalian evolution. This meta-analysis takes an initial step toward such a synthesis by collating available data and elucidating areas of promising future inquiry

Environment assessment by tadpoles and factors affecting anuran metamorphosis.

Anuran larvae show the ability to time their metamorphosis in response to environmental changes. Sensory modalities that allow tadpoles to assess the features of their environment, and subsequently mediate their developmental response, are not well understood. I analyzed whether visual and tactile features of conspecifics influence developmental response in anuran larvae. I exposed tadpoles of Rana, Bufo and Xenopus genera to enhanced tactile and visual cues by putting clay model tadpoles in the rearing water. Tadpoles that experienced both enhanced visual and tactile stimuli developed the fastest, and metamorphosed at the smallest body size. They showed the highest whole-body amount of stress hormone corticosterone. Developmental rate and hormone levels were the lowest in the control groups without any enhancement. This implies that tadpoles rely on both vision and mechanoreception for habitat assessment. They experience enhanced stimuli as stressful ones, and probably mediate environmental changes into developmental response via corticosterone.The use of vision was further examined in Rana and Bufo tadpoles. The aim was to determine whether larval anurans use images of other tadpoles as visual cues in assessing conspecifics density. Both real, and increased density simulated with mirrors, decreased tadpole growth and development, and increased activity. Thus, images of conspecifics are used as visual cues in tadpole's habitat assessment, and they induce phenotypic shifts in tadpoles' development and behaviour. Such ability to dissociate growth and developmental rates allows tadpoles adaptive response to habitat changes.I examined the extent to which dissociation is possible in my study of rare giant Xenopus laevis larvae. These giants lack thyroid glands and arrest their development at an early hindlimb bud stage. They continue to grow, developing into grossly deformed giants. They have excessive axial muscle mass, hypertrophied fat bodies, partially solidified lungs, and are negatively buoyant. Nevertheless, their gonads are mature, containing eggs and sperm. Gonadal development decoupled from metamorphosis brings giant Xenopus larvae closest of any anurans to being neotenic. However, under thyroid hormone treatment giants show some metamorphic changes, but all die at the stage when tail starts resorbing. I suggest that disproportionate growth in giant larvae precludes their complete metamorphosis.Thesis (Ph.D.)--Dalhousie University (Canada), 2004