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

Abstract

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.

Loss leads to gain

Hummingbirds display true hovering flight, an incredibly energy-intensive activity. Although much is known about the physiology of this movement, little has been known about the genetics underlying its evolution. Osipova et al . screened newly generated and previously sequenced bird genomes to search for key changes facilitating this high-energy locomotion. They found that a gluconeogenic muscle enzyme, FBP2, was lost as hovering flight evolved. Knockouts of this gene in avian cell lines led to an increase in glycolysis, mitochondria production, and mitochondrial respiration, all leading to higher energy efficiency. These results also illustrate how the loss of a gene can be adaptive. —SNV

Abstract

FBP2 loss in hummingbirds coincided with the evolution of true hovering flight and likely contributed to muscle adaptations.