Longevity and environmental temperature modulate mitochondrial DNA evolution in fishes

The link between longevity and mitochondrial function has been documented for years. Since mitochondrial DNA (mtDNA) encodes for electron transport system (ETS) proteins, we could suspect that its evolution is linked with that of longevity. A negative relationship has been documented between the synonymous substitution rate and lifespan when analyzing the whole mitochondrial genome in animals. In this study, we aimed to confirm this negative correlation for each of the mitochondrial protein coding genes (mtPCGs) and explore potential relationships between adaptation to extreme temperatures and the evolution of mtDNA. To this end, we selected 112 species of fish with a wide range of longevity as well as divergences in environmental temperature, which is a good proxy for energy metabolism in these animals. Our results 1) challenge the “rate of living” theory by not showing any correlation between longevity and environmental temperature, 2) confirm the negative relationship between substitution rate and longevity for each of the 13 mtPCGs, and 3) highlight for the first time a link between high conservation of the three COX genes and adaptation to warmer temperatures in fish. By challenging a paradigm and extending the conclusions made for mtDNA to individual genes, our study opens a wide field to be explored concerning study of the aging process. Moreover, the specific link between the evolution of COX genes and temperature tolerance confirms the importance of complex IV in adaptation to extreme temperatures and, more generally, the importance of distinguishing gene families when studying mtDNA evolution in animals.