A multiscale approach reveals elaborate circulatory system and intermittent heartbeat in velvet worms (Onychophora)

An antagonistic hemolymph-muscular system is essential for soft-bodied invertebrates. Many ecdysozoans (molting animals) possess neither a heart nor a vascular or circulatory system, whereas most arthropods exhibit a well-developed circulatory system. How did this system evolve and how was it subsequently modified in panarthropod lineages? As the closest relatives of arthropods and tardigrades, onychophorans (velvet worms) represent a key group for addressing this question. We therefore analyzed the entire circulatory system of the peripatopsid Euperipatoides rowelli and discovered a surprisingly elaborate organization. Our findings suggest that the last common ancestor of Onychophora and Arthropoda most likely possessed an open vascular system, a posteriorly closed heart with segmental ostia, a pericardial sinus filled with nephrocytes and an impermeable pericardial septum, whereas the evolutionary origin of plical and pericardial channels is unclear. Our study further revealed an intermittent heartbeat-regular breaks of rhythmic, peristaltic contractions of the heart-in velvet worms, which might stimulate similar investigations in arthropods.