Trematodes with a reproductive division of labour: heterophyids also have a soldier caste and early infections reveal how colonies become structured

• Published in: International journal for parasitology 2017-01, Vol.47 (1), p.41-50
• Main Authors: Garcia-Vedrenne, Ana E., Quintana, Anastasia C.E., DeRogatis, Andrea M., Dover, Christina M., Lopez, Maribel, Kuris, Armand M., Hechinger, Ryan F.
• Format: Article
• Language: English
• Subjects: Animals; Behavior, Animal; Biodiversity; California; Colony; Defence; Digenea; Echinostomatidae - anatomy & histology; Echinostomatidae - classification; Echinostomatidae - physiology; Heterophyidae - anatomy & histology; Heterophyidae - classification; Heterophyidae - physiology; Rediae; Reproduction - physiology; Snails - parasitology; Social Behavior; Sociality; Soldier caste; Species Specificity; Trematoda; Trematoda - pathogenicity; Trematoda - physiology; Trematode Infections - parasitology
• ISSN: 0020-7519; 1879-0135
• DOI: 10.1016/j.ijpara.2016.10.003

[Display omitted] •Morphological, distributional and behavioural patterns indicate that members of the Heterophyidae have a soldier caste.•A soldier caste is present in at least two superfamilies of the Trematoda: Echinostomatoidea and Opisthorchioidea.•A non-reproductive soldier caste is present in species that are lower in dominance hierarchies than previously known.•Developing infections are dominated by immature reproductives, and characterised by unimodal size-frequency distributions.•The size-frequency distributions become more bimodal as the colony ages. Recent findings have extended the documentation of complex sociality to the Platyhelminthes, describing the existence of a reproductive division of labour involving a soldier caste among the parthenitae of trematode parasites. However, all species examined to date occupy high positions in trematode interspecific dominance hierarchies and belong to two closely related families, the Echinostomatidae and the Philophthalmidae (Superfamily Echinostomatoidea). Further, the two species documented as lacking soldiers also belong to the Echinostomatidae. Here, we examine four species of intermediate dominance, all belonging to the family Heterophyidae (Superfamily Opisthorchioidea): Euhaplorchis californiensis, Phocitremoides ovale, Pygidiopsoides spindalis and Stictodora hancocki, all of which infect the California horn snail, Cerithideopsis californica (=Cerithidea californica). We quantify morphology, distribution and behaviour of rediae from fully developed colonies. We also provide information on colony structure for three developing heterophyid colonies to better understand colony development. We discuss the implications of our findings, particularly with respect to how they suggest alternatives to the conclusions of other researchers concerning the nature of trematode sociality. Our analyses of morphological, distributional and behavioural patterns of developed colonies indicate that these heterophyid trematodes have a non-reproductive caste whose function is defence of the colony from invading trematodes. Hence, a soldier caste occurs for species lower in dominance hierarchies than previously known, and is present in at least two superfamilies of digenean trematodes, suggesting that selection for a soldier caste may be much more common among the Trematoda than previously recognised.