Abstract

A fundamental question in biology is to uncover the mechanisms underlying how conserved signalling molecules generate diversified morphologies. It has been shown that a conserved Bone Morphogenetic Protein (BMP) type-ligand Decapentalegic (Dpp) functions as a wing vein determinant in the fruit fly, however it remains unknown how “diffusible” Dpp specifies elaborate and diversified insect wing vein patterns. Here we show that tightly controlled extracellular distribution of Dpp, rather than its expression pattern, correlates with complex wing vein patterns in two distantly related species, the Dipteran Drosophila melanogaster (fruit fly) and the Hymenopteran Athalia rosae (sawfly). In Drosophila , directional diffusion and active retention of Dpp localize the signal in future wing veins through BMP binding proteins, Short gastrulation (Sog) and Crossveinless (Cv), and through BMP type I receptor Thickvein (Tkv) and unknown positive feedback mechanisms, respectively. In sawfly, Dpp signal also reflects more complex wing vein patterns and loss of Cv by RNAi fails to establish both distinct fore- and hind-wing vein patterns. These results suggest that diversified insect wing vein patterns are acquired through directional Dpp diffusion at the extracellular space. Changes in extracellular regulation of secreted growth factors may be a general mechanism for creating evolutionarily diversified patterns.

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