Limb proportions show developmental plasticity in response to embryo movement

TLDR

Animals have evolved limb proportions adapted to different environments, yet the extent to which prenatal environmental factors such as embryo movement influence these proportions remains unclear. The study tests whether changes in prenatal movement driven by environmental factors alter embryonic limb growth and proportions. The authors used chick embryos to combine histology, immunochemistry, cell‑proliferation labeling, and unbiased array profiling to assess growth‑plate organization and identify cellular and transcriptional targets of embryo movement. Incubation temperature and pharmacological immobilization demonstrate that embryo movement modulates limb proportions by selectively regulating chondrocyte proliferation in specific growth plates via mTOR signaling, revealing how environmental factors shape prenatal bone growth.

Abstract

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.