Lineage-Associated Dichotomous Patterns in Codon Usage of Parasitic Cestodes

Genome remodeling, accompanied by modifications in base composition and translational architecture, may systematically reshape codon usage patterns, contributing to adaptation to changing biological demands through altered translational efficiency. In the present study, codon usage and genomic tRNA profiles were comparatively investigated in species representing two cestode lineages with contrasting genome organizations and biological characteristics. Despite relatively well-preserved amino-acid frequencies, these cestode species exhibited clear inter-lineage divergence in synonymous codon usage. Diphyllobothriideans preferentially utilized C-ending synonymous codons, whereas cyclophyllideans favored the corresponding T-ending alternatives, forming distinct lineage-associated codon dialects. These divergent patterns were consistently retained across coding-sequence datasets ranging from genome-wide to highly curated orthologous sets. Nucleotide composition contributed substantially to codon usage, while multiple lines of evidence indicated additional selective and translational constraints. Genomic tRNA gene pools were greatly reduced in cyclophyllideans, particularly taeniids. However, relationships between synonymous codon preferences and corresponding tRNA gene counts varied among codon families, indicating that their evolutionary associations may not be uniform. Collectively, these findings suggest that distinct codon usage patterns have evolved in cestode lineages with contrasting genomic architectures, shaped by lineage-specific compositional environments and, potentially for certain codon families, translational factors. They provide a framework for investigating how such diversifications contribute to translational adaptation to nutritional and environmental changes.