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 remains poorly understood in Heteroptera. Using serial semithin sections, microCT, and three dimensional reconstructions, we surveyed antennal circulatory organs in representatives of the major heteropteran infraorders. This analysis reveals exceptional structural and functional disparity, unmatched among the major insect clades investigated to date. In most examined taxa, each organ comprises an ampulla located inside the head capsule, from which an antennal vessel extends into the corresponding antenna. The presence, attachment sites, and functional role of associated muscles, however, vary markedly. In Gerromorpha, a dilator muscle expands the elastic ampulla before recoil drives hemolymph flow, whereas in Pentatomomorpha and Cimicomorpha, lineage specific compressor muscles compress the ampulla before elastic recoil refills it. In Enicocephalomorpha, no pumping muscle was detected, indicating a non pulsatile ampulla–vessel arrangement. By contrast, the examined Nepomorpha lack ampullae and antennal vessels; instead, a longitudinal diaphragm subdivides the antennal hemocoel into two compartments, enabling countercurrent hemolymph flow. Comparative analysis indicates that pulsatile ampulla–vessel circulatory systems (”antennal hearts”) represent the plesiomorphic condition in Heteroptera. Secondary transformations produced non pulsatile variants, diaphragm based circulation, and complete disappearance of antennal circulatory organs. These transformations are associated with reductions in antennal size and with cranial reorganizations linked to the evolution of piercing sucking mouthparts. Together, these findings establish heteropteran antennal circulatory organs as simple yet tractable model systems for understanding how structural reduction, functional shifts, and cranial reorganization shape organ diversification and loss.