Insufficient wing development possibly contributes to flightlessness of the silkworm Bombyx mori during domestication

The silkworm Bombyx mori is a fully domesticated insect and has lost its flight capability during domestication. However, it does not show obvious degradation of wing, rendering the mechanism of flightlessness elusive. In this study, we demonstrated that B. mori showed insufficient wing disc developmental properties, weaker adult wings and loosely arranged flight muscles with smaller cell size and relatively weaker wing flapping frequency, compared with Bombyx mandarina. Consistently, switch of transcriptomic landscape from larval to pupal wing discs occurred earlier in B. mori, with an earlier repression of genes related to development of wing and flight muscle precursor cells, as well as of those genes functioning in chromosome remodelling during metamorphosis. Knockout of the wing-disc expressing and the well-documented flight muscle gene fln caused loosely arranged flight muscles and reduced flight capacity. Meanwhile, core mitochondrial genes CoxI and CoxIII were downregulated in B. mori, accompanied by upregulation of CoxII and CoxIV and activated adverse cellular constituents such as reactive oxygen species, suggesting a possible functional impairment in the mitochondria of B. mori wing disc cells compared with those of B. mandarina. The results indicate that the flight system of B. mori has been structurally and functionally weakened by domestication and provide new insights into understanding behavioural domestication and insect flight from the developmental view.