Changes in body organ morphology have allowed animals to better exploit diverse habitats. As morphogenesis in general and organogenesis in particular are under genetic control, genetic modifications provide the basis for a wide range of morphologies. Our knowledge of the genetic basis of phenotypic diversification in evolution has focused mostly on quantitative traits. However, it is not clear how simple genetic changes can account for the coordinated variations that give rise to modified functional organs. Here we addressed this issue by analysing the expression and function of regulatory genes in the developing tracheal systems of two insect species. The larval tracheal system of Drosophila can be distinguished from the less derived tracheal system of the beetle Tribolium by two main features. First, the lateral spiracles, which in Tribolium connect the tracheal branches to the exterior in each segment, are not present in Drosophila. Instead, Drosophila has only one pair of strongly derived posterior spiracles. Second, the dorsal trunks, two prominent branches that distribute air from the posterior spiracles and extend longitudinally through the larva, are not present in Tribolium. Both innovations, while considered different structures, are functionally dependent on each other and linked to habitat occupancy. In this regard, buried Drosophila larvae in semi-liquid environments keep their posterior spiracles above the surface and distribute the gas along the body via the dorsal trunks. Conversely, the lateral spiracles of free-living Tribolium larvae provide sufficient airflow to all segments making unnecessary the formation of thick dorsal trunks. Here we show that changes in the domains of spalt and cut expression are associated with the acquisition of each innovation. Moreover, we show that these two genetic modifications are connected both functionally and genetically, thus providing an evolutionary scenario by which a genetic event contributes to the joint evolution of functionally interrelated structures.
- Received January 8, 2016.
- Accepted August 12, 2016.