Mechanoadaptation of developing limbs: shaking a leg

Abstract

The proportion of total limb length taken up by the individual skeletal elements (limb proportionality), varies widely between species. These diverse skeletal forms have evolved to allow for a range of limb uses and they first emerge as the embryo develops, to achieve the characteristic skeletal architecture of each species. During this time, the developing skeleton experiences mechanical loading as a result of embryonic muscle contraction. The possibility that adaptation to such mechanical input may allow embryos to coordinate the appearance of skeletal design with their expanding range of movements has so far received little attention. This is surprising, given the critical role exerted by embryo movement in normal skeletal development; stage-specific in ovo immobilisation of embryonic chicks results in joint contractures and a reduction in longitudinal bone growth in the limbs. Epigenetic mechanisms allow for selective activation of genes in response to environmental signals, resulting in the production of phenotypic complexity in morphogenesis; mechanical loading of bone during movement appears to be one such signal. It may be that 'mechanosensitive' genes under regulation of mechanical input adjust proportionality along the bone's proximo-distal axis, introducing a level of phenotypic plasticity. If this hypothesis is upheld, species with more elongated distal limb elements will have a greater dependence on mechanical input for the differences in their growth, and mechanosensitive bone growth in the embryo may have evolved as an additional source of phenotypic diversity during skeletal development.

Keywords: embryo movement; epigenetics; limb development; mechanical loading.

Figure 1

Variations in limb element proportionality – the proportion of total limb length taken up by the individual limb elements – between species. In species adapted for rapid terrestrial locomotion such as the ostrich (B) and jerboa (D) there is a tendency towards relative elongation of the distal and reduction of the proximal limb elements.

Figure 2

Reduced longitudinal growth of chicken embryo limb elements following in ovo immobilisation between E10–11, 10–14 and 10–18. Normal limb elements are represented by solid arrows and immobilised elements by outlined arrows. Percentage reductions in element length are given, except for E10–11 limbs where no significant reduction was reported. Data from Lamb et al. (2003) and Pitsillides (2006). Immobilisation prior to E14 appears to have little effect on growth.

Figure 3

Schematic showing the likely impact of in ovo immobilisation on the proportions of an ostrich limb, assuming the same pattern of reduced longitudinal growth reported in embryonic chickens immobilised from E10–18. (A) Normal ostrich limb. (B) Predicted effect of immobilisation on an ostrich limb. (C) Normal chicken limb. Immobilisation may alter ostrich limb proportions, resulting in a limb which appears more ‘chicken-like’.