ABSTRACT

The world is full of a fascinating diversity of life. Understanding the mechanism that has driven (and continues to drive) this amazing diversity is important, not only for science, but also for life itself. Knowledge of the history of life affects our way of thinking, our culture, and our society. Only recently, scientists have finally begun to understand how new body structures (novel structures) emerge during evolution. This project uses a core example of this novelty to explore a century-long question; where did the insect wing come from? Acquisition of wings has allowed the tremendously successful expansion of insects over the globe. However, the origin of insect wings remains a mystery and is regarded as a chief conundrum in biology. Through molecular and developmental analyses, wing-related tissues will be identified from a wide set of insects and other arthropods, which will allow for a reconstruction of the evolutionary history of insect wings. Gaining a comprehensive view of insect wing evolution will in turn advance our knowledge of the developmental basis underlying the development of new structures in general. The research will also further establish several organisms as alternative models for further genetic studies. In addition, this project will enhance undergraduate science education through establishing an infrastructure for student-oriented crowdsourcing efforts allowing researchers and students to publicly share the results of their gene disruption analyses and thus facilitate collaboration opportunities.

Over a century of debates and observations have culminated into two prominent hypotheses on the insect wing origin. One hypothesis, termed the paranotal hypothesis, connects the origin to the lateral extension of the dorsal thorax, the paranotal lobe. The second hypothesis, the exite hypothesis, connects the origin to the proximal leg segments and the branches (exites) stemming from these segments. Despite accumulating efforts to unveil the origin of insect wings, neither hypothesis has been able to surpass the other. A previous analysis in the Tomoyasu laboratory using Tribolium beetles has led to a combinational wing origin hypothesis, which states that insect wings have a dual origin, and that the merger of two unrelated tissues has been a key step in developing this morphologically novel structure during evolution. Further evidence for this hypothesis will be explored via (i) elucidating how the two tissues merge to form a complete wing structure in Tribolium, and (ii) identifying wing (serial) homologs from three additional species (a diving beetle, a cockroach, and a crustacean) to gain support of the hypothesis from a wider taxonomic breadth. RNA interference and expression analyses, along with CRISPR/Cas9-based genome editing techniques, will be used to identify and follow the development of wing-related tissues in these organisms. The morphological comparison of the identified wing (serial) homologs in these organisms with those of Tribolium, as well as with the proposed wing origins will allow for the construction of a more complete history of the evolution of insect wings.

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