Experimental demonstration of functional divergence in mitochondrial metabolism between two finch subspecies subjected to a thermal challenge

Whilst there is a growing appreciation that mitochondrial divergence across lineages is not selectively neutral, less work has examined the functional differences that may exist in closely divergent taxa. We measured mitochondrial oxygen consumption in the blood of two subspecies of an Australian songbird—the long-tailed finch, Poephila acuticauda—before and after 10 days of heat treatment at 40 °C to explore mitochondrial metabolic plasticity in response to thermal stress. There were significant differences between subspecies in the efficiency of oxidative phosphorylation, with P. a. hecki having higher energy production efficiency than P. a. acuticauda independent of heat treatment. Mitochondrial metabolism increased significantly after the treatment in 4 out of 6 variables in both subspecies, with P. a. hecki showing higher oxygen consumption rates in acclimating to 40 °C. In the same experiment, we also measured circulating levels of corticosterone to assess the effect of the treatment on stress and to explore a possible mechanistic link with mitochondrial metabolism. The heat significantly increased baseline corticosterone, but at an individual level, corticosterone and mitochondrial metabolism were unrelated, indicating that functional plasticity in response to the thermal challenge was not mechanistically determined by corticosterone. Whilst the geographic ranges of the 2 subspecies differ in climate, the extent to which the functional divergence in mitochondrial efficiency reflects selectively neutral or adaptive divergence requires further research. Nonetheless, the reduced metabolic flexibility of P. a. acuticauda after heat suggests that future increases in the frequency and intensity of heatwaves may impose asymmetric effects on the 2 subspecies.