Linking warmer nest temperatures to reduced body size in seabird nestlings: Possible mitochondrial bioenergetic and proteomic mechanisms

Rapid reduction of body size in populations responding to global warming suggests the involvement of temperature-dependent physiological adjustments during growth, such as mitochondrial alterations in the efficiency of producing metabolic energy, a process that is poorly explored, especially in endotherms. Here, we examined the mitochondrial metabolism and proteomic profile of red blood cells in relation to body size and cellular energy production in nestling shearwaters (Calonectris diomedea) developing at different temperatures. Despite not spending more energy to thermoregulate (invariant cell metabolic rate), their mitochondria had a higher inefficiency in coupling metabolism to energy production, as evidenced by bioenergetic and proteomic analyses. Mitochondrial inefficiency was positively related to cellular stress represented by heat shock proteins, antioxidant enzymes, and markers of mitochondrial stress. The observed temperature-related mitochondrial inefficiency was associated with reduced beak size and body mass and was linked to the downregulation of cellular growth factors and growth promoters determining body size. Nestlings of warmer nests had lighter bodies and smaller beaks at fledging. By analyzing the links between environmental temperature, mitochondrial inefficiency, and body size we discuss the physiological alterations that free-living birds, and probably other endotherms, need to trigger to cope with a warming world.