Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Hummingbirds possess distinct metabolic adaptations to fuel their energy-demanding hovering flight, but the underlying genomic changes are largely unknown. Here, we generated a chromosome-level genome assembly of the long-tailed hermit and screened for genes that have been specifically inactivated in the ancestral hummingbird lineage. We discovered that FBP2 (fructose-bisphosphatase 2), which encodes a gluconeogenic muscle enzyme, was lost during a time period when hovering flight evolved. We show that FBP2 knockdown in an avian muscle cell line up-regulates glycolysis and enhances mitochondrial respiration, coincident with an increased mitochondria number. Furthermore, genes involved in mitochondrial respiration and organization have up-regulated expression in hummingbird flight muscle. Together, these results suggest that FBP2 loss was likely a key step in the evolution of metabolic muscle adaptations required for true hovering flight.

Automated summary

Hummingbirds have specific metabolic adaptations for their energy-demanding hovering flight, but the genomic changes responsible for these adaptations are not well understood. In this study, researchers generated a high-quality genome assembly of the long-tailed hermit hummingbird and identified a gene called FBP2 that was inactivated during the evolution of hovering flight. Knocking down FBP2 in avian muscle cells increased glycolysis and mitochondrial respiration, as well as the number of mitochondria. Additionally, genes related to mitochondrial respiration and organization were up-regulated in hummingbird flight muscle. These findings suggest that the loss of FBP2 was a key step in the evolution of the metabolic muscle adaptations necessary for true hovering flight.