Genome-Wide Characterization of Four Gastropod Species Ionotropic Receptors Reveals Diet-Linked Evolutionary Patterns of Functional Divergence

Abstract

Ionotropic receptors (IRs) are a divergent subfamily of ionotropic glutamate receptors (iGluRs) that detect olfactory and environmental cues, influencing behaviors such as foraging and adaptation. To explore the evolution of IRs in relation to feeding ecology, we identified IRs and iGluRs from the genomes of four gastropods with distinct diets: <i>Pomacea canaliculata</i> (9 IRs/18 iGluRs), <i>Bellamya purificata</i> (10/22), <i>Cipangopaludina chinensis</i> (11/23), and <i>Babylonia areolata</i> (22/41). IRs were markedly expanded in <i>B. areolata</i>, suggesting lineage-specific diversification. Phylogenetic analysis grouped IRs and iGluRs into three clades, with IRs clustered with GluD, supporting early functional divergence following gene duplication. In all species, <i>IR25b</i> showed tandem duplication and played a central role in protein-protein interaction (PPI) networks. Most IRs were acidic, whereas IR-A and IR-C subgroups were basic, suggesting functional specialization among subfamilies. Structural analysis showed that IRs share conserved domains and motifs across species. Most IRs experienced purifying selection, while <i>P. canaliculata</i> showed relaxed constraints, suggesting weaker functional limitation. Collinearity analysis identified conserved genes, such as <i>BarIR-A.6</i> and <i>BarIR-D.1</i>, across species. qPCR confirmed tissue-specific expression of IRs in multiple organs. Together, these results reveal the molecular features and evolutionary patterns of IRs in gastropods, highlighting their potential roles in olfaction and dietary adaptation.

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