Antennal circulatory organs in Heteroptera: evolutionary diversification within a conserved functional framework

In insects, hemolymph flow through the antennae is driven by accessory circulatory organs, yet their functional and evolutionary morphology remain poorly understood in Heteroptera. Using serial semithin sections, microCT, and three-dimensional reconstructions, we surveyed antennal circulatory organs across five heteropteran infraorders and uncovered an exceptional degree of structural and functional disparity unmatched among major insect lineages examined to date. Most taxa possess a pulsatile ampulla within the head capsule from which an antennal vessel arises, but the architecture and action of the associated pump muscles differ strikingly among lineages. In Gerromorpha, a dilator muscle expands the elastic ampulla, and elastic recoil drives hemolymph flow. In Pentatomomorpha and Cimicomorpha, by contrast, lineage-specific compressor muscles reduce the volumen of the ampulla, which subsequently refills by recoil. Enicocephalomorpha lack a detectable pump muscle, indicating a non-pulsatile ampulla-vessel system. Nepomorpha depart even more radically: ampulla and vessel are absent, and a longitudinal diaphragm subdivides the antennal lumen into two compartments that support countercurrent hemolymph flow. Comparative analysis indicates that pulsatile ampulla-vessel systems ("antennal hearts") represent the plesiomorphic condition in Heteroptera, whereas non-pulsatile systems, diaphragm-based circulation, and complete loss constitute secondary transformations. These shifts are associated either with antennal miniaturization or with cranial reorganizations linked to the evolution of the piercing-sucking apparatus. Together, Heteroptera demonstrate how a conserved circulatory function can be maintained through strikingly different structural solutions, providing an unusually clear example of organ diversification, transformation, and loss.