Seasonal cold induces divergent structural/biochemical adaptations in different skeletal muscles of Columba livia: evidence for nonshivering thermogenesis in adult birds

Abstract

Birds are endothermic homeotherms even though they lack the well-studied heat producing brown adipose tissue (BAT), found in several clades of eutherian mammals. Earlier studies in ducklings have demonstrated that skeletal muscle is the primary organ of nonshivering thermogenesis (NST) plausibly via futile calcium (Ca2+)-handling through ryanodine receptor (RyR) and sarco–endoplasmic reticulum Ca2+-ATPase (SERCA). However, recruitment of futile Ca2+-cycling in adult avian skeletal muscle has not been documented. Studies in mammals show remarkable mitochondrial remodeling concurrently with muscle NST during cold. Here, we wanted to define the mitochondrial and biochemical changes in the muscles in free-ranging adult birds and whether different skeletal muscle groups undergo similar seasonal changes. We analyzed four different muscles (pectoralis, biceps, triceps and iliotibialis) from local pigeon (Columba livia) collected during summer and winter seasons in two consecutive years. Remarkable increase in mitochondrial capacity was observed as evidenced from succinate dehydrogenase (SDH) and cytochrome c oxidase (COX) activity staining in all the muscles. Interestingly, fibers with low SDH activity exhibited greater cross-sectional area during winter in all muscles except iliotibialis and became peripherally arranged in individual fascicles of pectoralis, which might indicate increased shivering. Furthermore, gene expression analysis showed that SERCA, sarcolipin and RyR are up-regulated to different levels in the muscles analyzed indicating muscle NST via futile Ca2+-cycling is recruited to varying degrees in winter. Moreover, proteins of mitochondrial-SR-tethering and biogenesis also showed differential alterations across the muscles. These data suggest that tropical winter (∼15°C) is sufficient to induce distinct remodeling across muscles in adult bird.