Abstract
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.
Highlights
Life history theory is based on the idea that the schedule and duration of key events in an organism’s lifetime are shaped by natural selection to ensure the largest number of surviving offspring in the generation
Our results offer compelling evidence that basal, maximal uncoupled, and nonmitochondrial metabolic rate of cells from tropical birds is lower than that of cells from temperate birds, and that cells from tropical birds have a lower proton leak than do cells from temperate species
Paired Comparisons In comparative biology, most investigators attempt to avoid statistical problems associated with the lack of independence of data from closely related species by using one or more methods that take into account phylogenetic relatedness [47,48,49]
Summary
Life history theory is based on the idea that the schedule and duration of key events in an organism’s lifetime are shaped by natural selection to ensure the largest number of surviving offspring in the generation. These events, juvenile development, age of sexual maturity, age of first reproduction, number of offspring, level of parental investment, and the rate of senescence, are influenced by the abiotic and biotic environment of the organism [1]. Situated at the slow end of the pace of life axis, tropical birds have low annual reproductive output, high annual survival rate, small clutch sizes, slow growth of nestlings, and long post-fledgling dependency on parents [15,16,17,18,19,20,21], whereas temperate birds tend to cluster more at the fast end of the spectrum, with large clutch sizes and high rates of mortality
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