13Proc. Arthropod. Embryol. Soc. Jpn. 54, 13–14 (2022)Ⓒ 2022 Arthropodan Embryological Society of Japan
ISSN 1341–1527

Genetic Mechanisms Governing the Development of Polyphagan
Pothorax and Their Implications to the Evolutionary Origin ofInsect Wings＊
Yoshinori TOMOYASU, Kevin D. DEEM and Madison R. MOE
Department of Biology, Pearson Hall, Miami University, Oxford, OH 45056, USA
E-mail: tomoyay@miamioh.edu (YT)The evolutionary origin of insect wings has
been the subject of heated debates for centuries.
These debates have culminated into two contrasting
hypotheses: the tergal origin hypothesis and the pleuralorigin hypothesis (Clark-Hachtel and Tomoyasu,2016). However, despite accumulating efforts to unveil
the origin of insect wings (including developmental,taxonomical, and paleontological analyses), neither
hypothesis has been able to surpass the other. Throughinvestigations into the development of wing-related
tissues in a wide taxonomy of organisms (including
beetles, cockroaches, and crustaceans), we previously
obtained evidence supporting a third hypothesis, thedual origin hypothesis (Clark-Hachtel et al., 2013,2021; Linz and Tomoyasu, 2018; Clark-Hachtel andTomoyasu, 2020). Although this hypothesis has thepotential to unify the two competing wing origin
hypotheses, it requires rigorous testing from variousfields. We reasoned that a detailed genetic analysisof the tissues that are serially homologous to wings(wing serial homologs, WSHs) will help us further
decipher the evolutionary origin of insect wings. Our
genetic dissection of the prothoracic (T1) body walltissues in the red flour beetle (Tribolium castaneum)
revealed several intriguing aspects of WSHs. First,
we obtained evidence for the unique nature of the T1
pleural plates that we previously identified as WSHs;
they are genetically distinct from the tergal tissue but
are not serially homologous to the pleural plates inother thoracic segments (such as the episternum andepimeron). This outcome further supports the ideathat these pleural plates are serially homologous towings. Second, we found that the mode of Hox action
operating is distinct between the tergal and pleural
WSHs, with the identity of pleural WSHs depending onHox cofactors while tergal WSH identity is independentof Hox cofactors. Interestingly, Hox cofactors are＊known to be important for the proximal wing identity,
suggesting that the evolutionary contribution of pleuraltissues might be predominantly to the proximal portionof the wing. Third, through an enhancer analysis in
Drosophila and Tribolium, we identified several wing
enhancers that are also active in either terga or pleura ofprothorax in Tribolium. The overlapping expressions ofthese enhancers between wings and T1 WSHs suggest ashared transcriptional landscape between wings and thetwo proposed origin tissues, while the non-overlapping
aspect of these enhancers within T1 supports distinct
identities between the tergal and pleural T1 WSHs.
Taken together, these genetic differences between thetwo T1 WSH identified here provide a further support
for the evolutionary contribution of the two distinct
lineages of thoracic tissues to the emergence of insectwings.
References
Clark-Hachtel, C.M. and Y. Tomoyasu (2016) Exploring theorigin of insect wings from an evo-devo perspective.
Current Opinion in Insect Science, 13, 77–85. https://doi.
org/10.1016/j.cois.2015.12.005
Clark-Hachtel, C.M. and Y. Tomoyasu (2020) Two setsof candidate crustacean wing homologues and theirimplication for the origin of insect wings. Nature Ecology& Evolution, 4, 1694–1702. https://doi.org/10.1038/s41559020-1257-8.
Clark-Hachtel, C.M., D.M. Linz and Y. Tomoyasu (2013)
Insights into insect wing origin provided by functional
analysis of vestigial in the red flour beetle, Tribolium
castaneum. Proceedings of the National Academy ofSciences of the United States of America, 110, 16951–16956. https://doi.org/10.1073/pnas.1304332110.
Clark-Hachtel, C., A. Fernandez-Nicolas, X. Belles, andY. Tomoyasu (2021) Tergal and pleural wing-related
tissues in the German cockroach and their implication

Contribution to the symposium “Acquisition of Functional Diversity of Insects” in the 57th Annual Meeting of the Arthropodan EmbryologicalSociety of Japan, July 9–10, 2021, Ushiku-numa, Ibaraki, Japan.

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to the evolutionary origin of insect wings. Evolution& Development, 23, 100–116. https://doi.org/10.1111/ede.12372.
Linz, D.M. and Y. Tomoyasu (2018) Dual evolutionary
origin of insect wings supported by an investigationof the abdominal wing serial homologs in Tribolium.
Proceedings of the National Academy of Sciences theUnited States of America, 115, E658–E667. https://doi.
org/10.1073/pnas.1711128115.