Comparative Mitogenomics of Meiacanthus Blennies Reveals Venom System Evolution and Adaptive Traits

Meiacanthus is a genus of nemophine blennies with an oral venom system, which includes buccal venom glands and canine fangs, and its evolutionary origin remains poorly understood. Here, we sequenced complete mitochondrial genomes of Meiacanthus species and their closely related non-venomous species, and performed comparative genomic and phylogenetic analyses to explore Meiacanthus’ evolution. Phylogenetic reconstruction identified Meiacanthus as sister to the (Aspidontus + Petroscirtes) clade, and suggested a probable three-step evolutionary sequence for its oral venom system. Codon usage bias analysis revealed that both natural selection and nucleotide mutations influence nemophine codon usage, shaping a bias that likely plays a crucial role in translational efficiency and regulating mitochondrial gene function. We also identified a unique nemophine tRNA-Cys (GCA) with a degraded DHU loop, which is prompted to be associated with a corresponding shift in codon usage preference. Additionally, all mitochondrial protein-coding genes of Meiacanthus except Cytb exhibited positive selection, with ND4 and ND5 having positively selected sites, likely linked to elevated energy demands for toxin synthesis. Our findings provide the first mitogenomic evidence illuminating the evolutionary pathway of the oral venom system in Meiacanthus, offering crucial insights into the evolution of oral venom systems in non-tetrapod vertebrates.