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Limb proportions show developmental plasticity in response to embryo movement.

ABSTRACT: Animals have evolved limb proportions adapted to different environments, but it is not yet clear to what extent these proportions are directly influenced by the environment during prenatal development. The developing skeleton experiences mechanical loading resulting from embryo movement. We tested the hypothesis that environmentally-induced changes in prenatal movement influence embryonic limb growth to alter proportions. We show that incubation temperature influences motility and limb bone growth in West African Dwarf crocodiles, producing altered limb proportions which may, influence post-hatching performance. Pharmacological immobilisation of embryonic chickens revealed that altered motility, independent of temperature, may underpin this growth regulation. Use of the chick also allowed us to merge histological, immunochemical and cell proliferation labelling studies to evaluate changes in growth plate organisation, and unbiased array profiling to identify specific cellular and transcriptional targets of embryo movement. This disclosed that movement alters limb proportions and regulates chondrocyte proliferation in only specific growth plates. This selective targeting is related to intrinsic mTOR (mechanistic target of rapamycin) pathway activity in individual growth plates. Our findings provide new insights into how environmental factors can be integrated to influence cellular activity in growing bones and ultimately gross limb morphology, to generate phenotypic variation during prenatal development.

SUBMITTER: Pollard AS

PROVIDER: S-EPMC5292730 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Limb proportions show developmental plasticity in response to embryo movement.

Pollard A S AS Charlton B G BG Hutchinson J R JR Gustafsson T T McGonnell I M IM Timmons J A JA Pitsillides A A AA

Scientific reports 20170206

Animals have evolved limb proportions adapted to different environments, but it is not yet clear to what extent these proportions are directly influenced by the environment during prenatal development. The developing skeleton experiences mechanical loading resulting from embryo movement. We tested the hypothesis that environmentally-induced changes in prenatal movement influence embryonic limb growth to alter proportions. We show that incubation temperature influences motility and limb bone grow ...[more]

PMID: 28165010

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Project description:The capacity to compensate for environmental change determines population persistence and biogeography. In ectothermic organisms, performance at different temperatures can be strongly affected by temperatures experienced during early development. Such developmental plasticity is mediated through epigenetic mechanisms that induce phenotypic changes within the animal's lifetime. However, epigenetic modifiers themselves are encoded by DNA so that developmental plasticity could itself be contingent on genetic diversity. In this study, we test the hypothesis that the capacity for developmental plasticity depends on a species' among-individual genetic diversity. To test this, we exploited a unique species complex that contains both the clonal, genetically identical Amazon molly (Poecilia formosa), and the sexual, genetically diverse Atlantic molly (Poecilia mexicana). We predicted that the greater among-individual genetic diversity in the Atlantic molly may increase their capacity for developmental plasticity. We raised both clonal and sexual mollies at either warm (28°C) or cool (22°C) temperatures and then measured locomotor capacity (critical sustained swimming performance) and unforced movement in an open field across a temperature gradient that simulated environmental conditions often experienced by these species in the wild. In the clonal Amazon molly, differences in the developmental environment led to a shift in the thermal performance curve of unforced movement patterns, but much less so in maximal locomotor capacity. In contrast, the sexual Atlantic mollies exhibited the opposite pattern: developmental plasticity was present in maximal locomotor capacity, but not in unforced movement. Thus our data show that developmental plasticity in clones and their sexual, genetically more diverse sister species is trait dependent. This points toward mechanistic differences in how genetic diversity mediates plastic responses exhibited in different traits.

Project description:Background and methodsBoth the concept of 'brain-sparing' growth and associations between relative lower limb length, childhood environment and adult disease risk are well established. Furthermore, tibia length is suggested to be particularly plastic under conditions of environmental stress. The mechanisms responsible are uncertain, but three hypotheses may be relevant. The 'thrifty phenotype' assumes that some components of growth are selectively sacrificed to preserve more critical outcomes, like the brain. The 'distal blood flow' hypothesis assumes that blood nutrients decline with distance from the heart, and hence may affect limbs in relation to basic body geometry. Temperature adaptation predicts a gradient of decreased size along the limbs reflecting decreasing tissue temperature/blood flow. We examined these questions by comparing the size of body segments among Peruvian children born and raised in differentially stressful environments. In a cross-sectional sample of children aged 6 months to 14 years (n = 447) we measured head circumference, head-trunk height, total upper and lower limb lengths, and zeugopod (ulna and tibia) and autopod (hand and foot) lengths.ResultsHighland children (exposed to greater stress) had significantly shorter limbs and zeugopod and autopod elements than lowland children, while differences in head-trunk height were smaller. Zeugopod elements appeared most sensitive to environmental conditions, as they were relatively shorter among highland children than their respective autopod elements.DiscussionThe results suggest that functional traits (hand, foot, and head) may be partially protected at the expense of the tibia and ulna. The results do not fit the predictions of the distal blood flow and temperature adaptation models as explanations for relative limb segment growth under stress conditions. Rather, our data support the extension of the thrifty phenotype hypothesis to limb growth, and suggest that certain elements of limb growth may be sacrificed under tough conditions to buffer more functional traits.

Project description:While there is broad agreement that early hominins practiced some form of terrestrial bipedality, there is also evidence that arboreal behavior remained a part of the locomotor repertoire in some taxa, and that bipedal locomotion may not have been identical to that of modern humans. It has been difficult to evaluate such evidence, however, because of the possibility that early hominins retained primitive traits (such as relatively long upper limbs) of little contemporaneous adaptive significance. Here we examine bone structural properties of the femur and humerus in the Australopithecus afarensis A.L. 288-1 ("Lucy", 3.2 Myr) that are known to be developmentally plastic, and compare them with other early hominins, modern humans, and modern chimpanzees. Cross-sectional images were obtained from micro-CT scans of the original specimens and used to derive section properties of the diaphyses, as well as superior and inferior cortical thicknesses of the femoral neck. A.L. 288-1 shows femoral/humeral diaphyseal strength proportions that are intermediate between those of modern humans and chimpanzees, indicating more mechanical loading of the forelimb than in modern humans, and by implication, a significant arboreal locomotor component. Several features of the proximal femur in A.L. 288-1 and other australopiths, including relative femoral head size, distribution of cortical bone in the femoral neck, and cross-sectional shape of the proximal shaft, support the inference of a bipedal gait pattern that differed slightly from that of modern humans, involving more lateral deviation of the body center of mass over the support limb, which would have entailed increased cost of terrestrial locomotion. There is also evidence consistent with increased muscular strength among australopiths in both the forelimb and hind limb, possibly reflecting metabolic trade-offs between muscle and brain development during hominin evolution. Together these findings imply significant differences in both locomotor behavior and ecology between australopiths and later Homo.

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Limb proportions show developmental plasticity in response to embryo movement.

Publications

Limb proportions show developmental plasticity in response to embryo movement.

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