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

Abstract

We show that the globally invasive, human-infectious flatworm, <i>Haplorchis pumilio</i>, possesses the most physically specialized soldier caste yet documented in trematodes. Soldiers occur in colonies infecting the first intermediate host, the freshwater snail <i>Melanoides tuberculata</i>, 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 <i>H. pumilio</i> 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 <i>H. pumilio</i> 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, <i>H. pumilio</i> 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.