A muscle-centered hierarchical breakdown underlies flight loss during silkworm domestication

Area of Science:

• Evolutionary Biology
• Developmental Biology
• Genetics

Background:

• Recurrent loss of complex traits like insect flight provides insights into evolutionary regression.
• Domestication of the silkworm, Bombyx mori, from its flight-capable ancestor, B. mandarina, serves as a model for studying flight loss.

Purpose of the Study:

• To investigate the genetic and cellular mechanisms underlying the loss of insect flight during domestication.
• To identify conserved genetic modules involved in flight muscle development and function.

Main Methods:

• Integration of single-cell and spatial transcriptomics in developing flight organs of Bombyx species.
• Gene knockdown experiments in B. mandarina and perturbation of the Hippo pathway in B. mori.
• Comparative analysis of the genetic module in the migratory pest Helicoverpa armigera.

Main Results:

• Flight loss is a coordinated breakdown centered on flight muscle cells.
• Disintegration of a multi-tiered genetic module involving mitochondrial energy production, wing vein patterning, and flight muscle specification.
• The identified muscle-centric module is conserved in Helicoverpa armigera and its disruption impairs flight.

Conclusions:

• Trait degeneration, exemplified by flight loss, occurs as a muscle-centered collapse.
• A conserved genetic module controlling flight muscle development presents a potential target for precision pest control strategies.