Opposing insulin signals underlie the same developmental switch across hemipteran insects

Across metazoans, the insulin/insulin-like signaling (IIS) pathway is assumed to promote organ growth. We found that genes within the IIS pathway evolved opposite roles in organ growth across wing-dimorphic insects, playing opposite roles in regulating the developmental switch between short and long wings. In the firebug, the InR-Chico-PI3K-PDK1-Tsc1/2-TORC1 cascade redirects the switch from short to long wings by inactivating IIS, whereas in the planthopper, the InR-Chico-PI3K-Akt-FoxO cascade redirects this same switch by activating IIS. Activation or inactivation of IIS results in low ecdysteroid titers in both species by regulating different genes within the ecdysteroid biosynthesis pathway, which in turn induces long wing development. Our findings reveal a negative relationship between IIS and organ growth and a mechanism for how a hormone pathway can translate opposing IIS activities into the same developmental switch across species.