Tissue-specific mitochondrial pathway remodeling linked to longevity in honeybee queens

by Clément Joël Lucien Chevret, José Francisco Echegaray, Alexander Walton, Maryam Lo, Olav Rueppell, Hélène Lemieux

Mitochondrial metabolism plays a critical role in determining lifespan across animal taxa. In our study, we used the Western honeybee (Apis mellifera) as a model, capitalizing on the stark lifespan difference between queens, which often live more than two years, and summer workers, which survive only about 30 days, despite sharing the same genetic background. We investigated mitochondrial function in head tissue, thoracic muscle, and abdominal fat tissue of queens and workers, comparing early (7 days) and late adult stages (28–30 days in workers; 2 years in queens). No significant differences in mitochondrial flux control ratio for the NADH- Succinate- and glycerophosphate (Gp) pathways were found in thoracic muscles across castes or age groups. In head and abdominal fat tissues, early-life queens showed reduced reliance on NADH-linked pathways for maximal respiratory flux compared to workers. The decrease in the NADH-pathway was compensated by an increase in the Gp-pathway contribution. Queens exhibited reduced phosphorylation-pathway control over OXPHOS compared to workers, both in head tissue during early life and in abdominal fat tissue later in life. These findings reveal caste- and tissue-specific patterns of mitochondrial regulation that may contribute to dramatic lifespan divergence observed in eusocial insects. They suggest that early-life metabolic flexibility could play an important role in shaping life history evolution in Apis mellifera.