Cellular metabolic rate is influenced by life-history traits in tropical and temperate birds

• Published in: PloS one 2014-01, Vol.9 (1), p.e87349-e87349
• Main Authors: Jimenez, Ana Gabriela, Van Brocklyn, James, Wortman, Matthew, Williams, Joseph B
• Format: Article
• Language: English
• Subjects: Acidification; Animal metabolism; Animals; Basal Metabolism - physiology; Biological Evolution; Biology; Birds; Birds - physiology; Body size; Body Size - physiology; Cancer; Cell Respiration - physiology; Ecology; Environment; Evolution; Fibroblasts; Fibroblasts - physiology; Glucose metabolism; Glycolysis; Glycolysis - physiology; Life Cycle Stages - physiology; Life history; Longevity - physiology; Medicine; Metabolic rate; Metabolism; Mitochondria; Natural selection; Organismal biology; Oxidative stress; Oxygen Consumption - physiology; Phenotype; Phylogeny; Physiological aspects; Physiology; Rodents; Skin; Species; Stem cells; Tropical Climate
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0087349

In general, tropical birds have a "slow pace of life," lower rates of whole-animal metabolism and higher survival rates, than temperate species. A fundamental challenge facing physiological ecologists is the understanding of how variation in life-history at the whole-organism level might be linked to cellular function. Because tropical birds have lower rates of whole-animal metabolism, we hypothesized that cells from tropical species would also have lower rates of cellular metabolism than cells from temperate species of similar body size and common phylogenetic history. We cultured primary dermal fibroblasts from 17 tropical and 17 temperate phylogenetically-paired species of birds in a common nutritive and thermal environment and then examined basal, uncoupled, and non-mitochondrial cellular O2 consumption (OCR), proton leak, and anaerobic glycolysis (extracellular acidification rates [ECAR]), using an XF24 Seahorse Analyzer. We found that multiple measures of metabolism in cells from tropical birds were significantly lower than their temperate counterparts. Basal and uncoupled cellular metabolism were 29% and 35% lower in cells from tropical birds, respectively, a decrease closely aligned with differences in whole-animal metabolism between tropical and temperate birds. Proton leak was significantly lower in cells from tropical birds compared with cells from temperate birds. Our results offer compelling evidence that whole-animal metabolism is linked to cellular respiration as a function of an animal's life-history evolution. These findings are consistent with the idea that natural selection has uniquely fashioned cells of long-lived tropical bird species to have lower rates of metabolism than cells from shorter-lived temperate species.