Cenozoic Tectonics Ignite Mitochondrial Codon Innovations Propelling Canid Body Size Evolution and Transcontinental Radiations

The adaptive evolution of Canidae mitochondrial genomes and their mechanistic association with ecological strategies have long been constrained by insufficient cross-lineage integration and unresolved multidimensional interaction networks. Here, complete mitochondrial genomes from all extant canid species (including 11 newly assembled genomes) were analyzed, revealing highly conserved gene arrangements and lineage-specific codon usage patterns. High-altitude species exhibited atypical initiation codons for ND4L, while boreal species exhibited significant termination codon shifts, and polar specialists had distinct codon optimization profiles. Positive selection analyses identified strong selective pressures on arginine- and leucine-encoding sites, with core oxidative phosphorylation genes demonstrating accelerated adaptive evolution in large-bodied canids and specialized predatory lineages. Phylogenomic reconstructions revealed consistency in South American Lycalopex radiation timing with regional orogenic events, while also linking Canis diversification to grassland biome expansion. Further, statistical models confirmed robust correlations between mitochondrial evolutionary rates and both body mass and predatory ecology, wherein body size increases drive metabolic optimization through lineage-specific selection on energy-related genes. Based on these observations, a "functional constraint-geological driver-body size adaptation" tripartite framework is proposed that highlights how mitochondrial genomes maintain metabolic plasticity through mutation-selection equilibrium, how geological events trigger lineage divergence, and how body size-predation strategies shape modular gene evolution. Consequently, this study establishes a novel paradigm for understanding genome-environment interactions in terrestrial carnivore adaptations.