Tergal and pleural wing-related tissues in the German cockroach and their implication to the evolutionary origin of insect wings

This article also appears in: Evolution 2021, Evolution 2021 Virtual Issue.The acquisition of wings has facilitated the massive evolutionary success of pterygotes (winged insects), which now make up nearly three-quarters of described metazoans. However, our understanding of how this crucial structure has evolved remains quite elusive. Historically, two ideas have dominated in the wing origin debate, one placing the origin in the dorsal body wall (tergum) and the other in the lateral pleural plates and the branching structures associated with these plates. Through studying wing-related tissues in the wingless segments (such as wing serial homologs) of the beetle, Tribolium castaneum, we obtained several crucial pieces of evidence that support a third idea, the dual origin hypothesis, which proposes that wings evolved from a combination of tergal and pleural tissues. Here, we extended our analysis outside of the beetle lineage and sought to identify wing-related tissues from the wingless segments of the cockroach, Blattella germanica. Through detailed functional and expression analyses for a critical wing gene, vestigial (vg), along with re-evaluating the homeotic transformation of a wingless segment induced by an improved RNA interference protocol, we demonstrate that B. germanica possesses two distinct tissues in their wingless segments, one with tergal and one with pleural nature, that might be evolutionarily related to wings. This outcome appears to parallel the reports from other insects, which may further support a dual origin of insect wings. However, we also identified a vg-independent tissue that contributes to wing formation upon homeotic transformation, as well as vg-dependent tissues that do not appear to participate in wing formation, in B. germanica, indicating a more complex evolutionary history of the tissues that contributed to the emergence of insect wings.This study is supported by the Miami University Faculty Research Grants Program (CFR; to Yoshinori Tomoyasu), the National Science Foundation (NSF; IOS1557936 to Yoshinori Tomoyasu), an NSF Graduate Research Fellowship (to Courtney Clark-Hachtel), the Spanish Ministry of Economy and Competitiveness (including support for the visit of Ana Fernandez-Nicolas to the Tomoyasu lab; CGL2012-36251, CGL2015-64727-P, and PID2019-104483GB-I00 to Xavier Belles), the Catalan Government (2014 SGR 619, 2017 SGR 10c0 to Xavier Belles), and European Fund for Economic and Regional Development (FEDER funds to Xavier Belles).Peer reviewe