Abstract
Pectoralis phenotypic variation plays a fundamental role in locomotion and thermogenesis in highland birds. However, its regulatory and metabolic mechanisms remain enigmatic to date. Here, we integrated phenomic, transcriptomic, and metabolomic approaches to determine muscle variation and its underpinning mechanisms across altitudinal songbirds. Phenomics confirmed that all highland birds had considerable increases in muscle oxidative capacity, capillarity, and mitochondrial abundance in our study. Correspondingly, transcriptomic analyses found that differentially expressed genes in phenotype-associated modules enriched for blood vessel, muscle structure development, and mitochondrial organization. Despite similar traits and functional enrichments across highland birds, different mechanisms drove their occurrence in high-altitude tree sparrow and 2 snow finches. Importantly, a metabolic feature shared by all the 3 highland birds is the improvement in insulin sensitivity and glucose utilization through activating insulin signaling pathway, which is vital to increase muscle oxidative capacity and maintain metabolic homeostasis. Nevertheless, fatty acid biosynthesis and oxidation are enhanced in only 2 snow finches which had a long evolutionary history on the high plateau, also differing from ketone body metabolism in recently introduced colonizer of the tree sparrow of the high plateau. Our study represents a vital contribution to reveal the regulatory and metabolic basis of pectoralis variation across altitudinal songbirds.
Highlights
Pectoralis phenotypic variation plays a fundamental role in locomotion and thermogenesis in highland birds
Hypoxia and hypothermia are two significantly severe challenges to aerobic exercise and thermogenesis in small endotherms, because a high rate of O2 flux should be concurrently sustained to thermogenesis in cold temperature[1]
Physiological modifications, including typically greater capillary density, more oxidative fiber, and higher proportion of subsarcolemmal mitochondria have been found in pectoralis of highland birds [2]
Summary
This study was carried out in strict accordance with the recommendations of the Regulations for the Administration of Affairs Concerning Experimental Animals (Ministry of Science and Technology, China, revised in June 2004). All procedures performed on birds were approved by the Institute of Zoology Animal Care Committee. All birds were euthanized through cardiac compression, and all efforts were made to minimize suffering of animals. Wild birds were caught with mist-net in summer of 2016, highland bird populations from Qinghai Province about 3200 m (10 tree sparrows, Passer montanus) and 3900 m (10 rufous-necked snow finch, Pyrgilauda ruficollis and 10 white-rumped snow finch, Onychostruthus taczanowskii) and lowland population (n = 8) of the tree sparrow from Yanqi Lake of Beijing at 80 m (many details were represented in table S6). All birds were euthanized in 3–5 seconds through cardiac compression. Pectoral major muscle was dissected immediately following euthanasia, flash-frozen in liquid nitrogen and stored at -80 °C
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