The circulatory organs of insect wings: Prime examples for the origin of evolutionary novelties

Of all evolutionary events that are discussed as novelties, the origin of insect wings is perhaps the most frequently cited. Yet, the novelty discussion on this issue has almost exclusively focused on the dermal folds, which form the exterior parts of the wings. The involvement of the circulatory system, however, has been widely neglected despite its mandatory function in the development and maintenance of the wings. Here, we outline the multiple roles of the thoracic wing circulatory organs and discuss their morphological disparity in the light of evolutionary novelty. A modification of parts of the dorsal vessel is the simplest type of wing circulatory organ. It undoubtedly represents the plesiomorphic character state from which separate and completely autonomous wing-hearts evolved multiple times independently. Only these wing-hearts are considered to represent morphological novelties in a strict sense. This conclusion is supported by developmental studies in Drosophila whose wing-hearts originate from an independent pericardial cell lineage and are not individualized parts of the myocardium, as previously assumed. Remarkably, the regulatory gene network underlying wing-heart formation is unique, in that it is mainly somatic muscle-like, but also includes genes typical for cardiomyogenesis. Based on comparative analyses we conclude that the evolution of autonomous wing-hearts was triggered by spatial constraints inflicted by the rearrangement of the flight apparatus rather than by alterations in circulatory demands. Further, we point out that the integration of tergal structures in the evolution of wing circulatory organs supports the hypothesis of the involvement of paranotal elements in the emergence of wings. Taken together, we conclude that the various types of insect wing circulatory organs represent different degrees of body part individualization which serve as instructive prime examples to elucidate the origin of evolutionary novelties and the delimitation problems inherent to this topic.