Metabolic plasticity mediates differential responses to spring and autumn migrations: Evidence from gene expression patterns in migratory buntings.

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What is the central question of this study? What are the molecular underpinnings of seasonal metabolic plasticity during spring and autumn migrations in songbirds? What is the main finding and its importance? We report differences in mRNA levels of genes involved in the regulation of glucose and fat metabolism between photoinduced non-migratory and migratory states and between the spring and autumn migratory states. Higher expression of genes associated with fat mobilization and energy generation in the spring than in the autumn migration suggests differential activation of the metabolic pathways or alteration in the efficiency of existing functional machinery during annual journeys between nearly fixed destinations. The molecular underpinnings of metabolic plasticity underlying differential responses to spring and autumn migrations are not well understood. We investigated this by examining the differences in mRNA levels of metabolic genes in the liver, muscle and adipose tissues of night-migratory red-headed buntings between photostimulated non-migratory and migratory states and between spring and autumn migratory states. Buntings accumulated more subcutaneous fat and hepatic lipid, had higher body mass, larger adipose cells and higher circulating triglyceride and free fatty acid levels and exhibited more intense Zugunruhe in the spring migratory state than in the autumn migratory state. More importantly, we found differences in the hepatic expression of pdc and pdk genes, indicating a differential acetyl-CoA requirement, and of the mdh and ogdh genes, suggesting differential oxidative phosphorylation between the non-migratory and migratory states and between the spring and autumn migratory states. Differences in fasn, bmal1 and glut1 mRNA levels were consistent with this and suggested seasonal differences in lipogenesis and/or glucose uptake. Likewise, differences in mRNA levels of genes coding for lipases (atgl and lpl) suggested that adipose triglycerides and free fatty acids serve largely as the metabolic substrate. Furthermore, changes in mRNA levels of genes coding for the fatty acid binding protein (fabp3) and fatty acid translocases (cd36) were consistent with differential fat fuel supply (via circulating free fatty acids) to aerobically exercising flight muscles between the spring and autumn migrations. These results show seasonal adaptation of genetic pathway(s) underlying seasonal metabolic plasticity that seems to mediate differential responses to spring and autumn migrations in latitudinal migratory songbirds.