The physical soldier caste of an invasive, human-infecting flatworm is morphologically extreme and obligately sterile

We show that the globally invasive, human-infectious flatworm, Haplorchis pumilio, possesses the most physically specialized soldier caste yet documented in trematodes. Soldiers occur in colonies infecting the first intermediate host, the freshwater snail Melanoides tuberculata, and are readily distinguishable from immature and mature reproductive worms. Soldiers possess a pharynx five times absolutely larger than those of immature and mature reproductives, lack a germinal mass, and have a different developmental trajectory than reproductives, indicating that H. pumilio soldiers constitute a reproductively sterile physical caste. Neither immature nor mature reproductives showed aggression in in vitro trials, but soldiers readily attacked heterospecific trematodes that coinfect their host. Ecologically, we calculate that H. pumilio caused ~94% of the competitive deaths in the guild of trematodes infecting its host snail in its invasive range in southern California. Despite being a dominant competitor, H. pumilio soldiers did not attack conspecifics from other colonies. All prior reports documenting division of labor and a trematode soldier caste have involved soldiers that may be able to metamorphose to the reproductive stage and have been from nonhuman-infectious marine species; this study provides clear evidence for an obligately sterile trematode soldier, while extending the phenomenon of a trematode soldier caste to freshwater and to an invasive species of global public health concern.