Reduced specification of lateral plate mesoderm progenitors underpins heterochronic development of the emu wing

Abstract

AbstractBetween tetrapods the limbs have undergone considerable remodelling to achieve unique adaptive behaviours. The forelimb is an ideal model for exploring the molecular basis of adaptive limb development, as it shows remarkable structural variation and is accessible for experimental manipulation. Of the most striking alterations to limb shape is the evolution of powered flight in birds. However, subsequently the flightless ratites (Paleognathae) have further evolved multiple instances of wing reductions, each utilizing distinct molecular mechanisms and displaying heterochrony with flighted birds (Neoaves). The emu has evolved a greatly reduced wing, consisted of a single digit. Thus, the emu is an excellent model to comparatively determine the cellular and molecular basis of wing heterochrony. We utilize comparative single cell transcriptomics of the developing forelimb field in the emu and chicken, to identify the source of the emus reduced wing. This was observed to occur via reduced specification and commitment of lateral plate mesoderm limb progenitor cells, which was accompanied by differential gene expression, persisting during limb initiation and outgrowth. These data suggest a progenitor allocation model, whereby altered limb morphologies may be achieved through altered commitment of precursor cells which act as an underlying template for pre- and post-patterning mechanisms.