Mimicking the natural doping of migrant sandpipers in sedentary quails:effects of dietary n-3 fatty acids on muscle membranes and PPAR expression

Abstract

SUMMARYWild semipalmated sandpipers (Calidris pusilla) eat n-3 fatty acids to prime their muscles for long migrations. Sedentary bobwhite quails (Colinus virginianus) were used as a model to investigate the mechanisms for this natural doping. Our goal was to characterize the stimulating effects of n-3 eicosapentaenoic acid (EPA) and n-3 docosahexaenoic acid (DHA) on oxidative capacity. Mechanisms linked to changes in membrane composition and in gene expression for peroxisome proliferator-activated receptors (PPAR) were investigated. Dietary n-3 fatty acids stimulated the activities of oxidative enzymes by 58-90% (citrate synthase, cytochrome oxidase, carnitine palmitoyl transferase and hydroxyacyl dehydrogenase), and sedentary quails showed the same changes in membrane composition as sandpipers preparing for migration. EPA and DHA have the same doping effect. The substitution of n-6 arachidonic acid by n-3 EPA in membrane phospholipids plays an important role in mediating the metabolic effects of the diet, but results provide no significant support for the involvement of PPARs (as determined by changes in gene expression). The fatty acid composition of mitochondrial membranes and sarcoplasmic reticulum can be monitored by measuring total muscle phospholipids because all phospholipids are equally affected by diet. Only extreme regimes of endurance training can lead to increments in oxidative capacity matching those induced here by diet. As they prepare for long migrations, semipalmated sandpipers improve their physical fitness by eating! Choosing n-3 fatty acid doping over endurance training strikes us as a better strategy to boost aerobic capacity when rapid storage of energy is critical.

Western diet increases wheel running in mice selectively bred for high voluntary wheel running

“…43 Both fatty acids lead to an increased cellular membrane fluidity and serve as ligands for peroxisome proliferators-activated receptors, 44 which are involved in regulation of lipid metabolism. Different types of fatty acids, however, are not identical in their effects on performance 45 or health.…”

Obese super athletes: fat-fueled migration in birds and bats

“…Wintering and migratory western sandpipers showed strong positive correlations between plasma n-3 PUFA and pectoralis HOAD and CPT activities, but not CS activity or H-FABP protein content (Guglielmo, 2010). Further support for natural doping came from a dosing study of non-migratory bobwhite quail (Colinus virginianus), which responded to daily supplementation with oils high in 20:5n-3 (59%) and 22:6n-3 (70%) by increasing pectoralis activities of CS, CPT, HOAD and COX (Nagahuedi et al, 2009). However, it is not certain that the correlations measured in sandpipers represent cause and effect, or that the variation in muscle enzyme activities meaningfully affect flight performance.…”

Molecular networks in skeletal muscle plasticity

“…The authors relate this change to the consumption of an amphipod, containing high amounts of n-3 polyunsaturated fatty acids. In later laboratory experiments it was shown that unsaturated dietary fatty acids could increase oxidative enzymes by up to 90% in sedentary quail muscles, whereby observed functional changes were attributed to changes in membrane fluidity and PPAR expression (Nagahuedi et al, 2009). Observations on migratory birds further indicate that flight muscle mass changes seasonally by up to 40% in red knots, Calidris canutus, kept in captivity, under constant photoperiod and without evidence of exercise training (Dietz et al, 1999;Pierce and McWilliams, 2014).…”