Coordinated Evolution of Salivary Glands and Sialome in True Bugs: Dietary Adaptation and Venom Protein Co-option

Abstract

Dietary adaptations are fundamental drivers of evolutionary innovations. Still, the morphological and molecular mechanisms underlying these transitions remain poorly understood. True bugs (Heteroptera), one of the most diverse clades of hemimetabolous insects, have evolved a vast array of trophic niches. They exhibit remarkable structural and functional diversity in their salivary glands, providing an ideal system for investigating how dietary variation shapes evolutionary trajectories. Using morphometric, proteo-transcriptomic, and comparative phylogenetic approaches, we examined the evolutionary patterns of salivary glands across 220 hemipteran species, encompassing all seven infraorders and six dietary categories of Heteroptera. Our results reveal strong correlations between dietary shifts, salivary gland size and allometric scaling. Ancestral state estimation analysis demonstrates multiple evolutionary transitions in salivary gland morphology, highlighting structural adaptations associated with different diets. Furthermore, we found that distantly related species with similar diets share dominant salivary protein groups, implying convergent molecular solutions to shared feeding challenges. Notably, we identify venom protein family 2 as a key adaptation. This family originated through lineage-specific co-option of an ancestral protein into heteropteran salivary systems, followed by extensive expansion that facilitated dietary diversification. These findings provide novel insights into the morphological, physiological, and molecular adaptations of salivary glands, emphasizing the dynamic interplay between feeding ecology and macroevolution.