Sensing Underwater: Diversifying Selection, Convergent Evolution and Inactivation in Sensory Receptors' Genes of Aquatic Mammals.

Cetaceans and sirenians independently transitioned from land to water, evolving unique and convergent sensory adaptations shaped by aquatic environments. Among sensory receptors, the Transient Receptor Potential (TRP) channel superfamily is central to thermo-, chemo-, and mechanosensation, but its evolutionary history in fully aquatic mammals remains poorly characterized. Here, we investigated the molecular evolution of TRP channels in these lineages. Orthology and phylogenetic relationships were inferred using Maximum Likelihood and Bayesian approaches. Signals of positive selection and molecular convergence were evaluated with codon and amino acid models. Amino acid substitutions, protein structure, and stability were assessed using 3D protein modeling. Our analyses reveal accelerated evolutionary rates in aquatic mammals, including multiple positively selected sites, lineage-specific amino acid substitutions, and convergent evolution across cetaceans and sirenians. Protein-level assessments identified substitutions with potential functional consequences, and evidence of pseudogenization was detected in cetacean PKD1L3, PKD2L1, TRPA1, and TRPM5, in contrast to intact copies in sirenians. These patterns suggest lineage-specific sensory trajectories, including reduced chemosensory repertoires in cetaceans, conservation of taste-related genes in sirenians, and adaptations in somatosensory associated genes that reflect both convergent requirements of fully underwater living and distinct aquatic environments. Overall, our findings advance understanding of the molecular mechanisms underlying sensory evolution during the land-to-water transition in mammals.