Self-sustaining infrapopulation or colony? Redial clonal groups of Himasthla elongata (Mehlis, 1831) (Trematoda: Echinostomatidae) in Littorina littorea (Linnaeus) (Gastropoda: Littorinidae) do not support the concept of eusocial colonies in trematodes

Abstract

Abstract:Trematode sporocysts and rediae reproduce by parthenogenesis, forming clonal groups in the molluscan host. It has recently become popular to consider these groups as eusocial colonies, with division of labour between rediae morphs: small 'soldiers' incapable of reproduction defend the colony, while large rediae reproduce. Alternatively, clonal groups can be considered as self-sustaining infrapopulations. We tested these two hypotheses in the light of new data on rediae of Himasthla elongata (Mehlis, 1831) from snails Littorina littorea (Linnaeus) concerning ultrastructure, growth character and composition of their groups. Clonal groups under study contained rediae of different age and maturity stages: small (young) rediae, rediae with early cercarial embryos, rediae with late embryonic cercariae, rediae with fully formed motile cercariae, rediae with redial embryos and degenerating rediae. Small rediae had a reproductive organ, the germinal mass, whereas most large rediae with developing cercariae did not, which contradicts the eusocialconcept. Overall distribution of rediae by size and by gut to body length ratio was bimodal, which agrees with the eusocial concept ('soldiers' and 'reproductives' as modal size classes). On closer inspection, however, the bimodal size-frequency distributions (SFD) turned out to be the sum of unimodal SFD of rediae at various stages of maturity. The overall bimodality was determined by the character of redial growth resulting in a relatively low occurrence of intermediate morphs and by the developmental arrest in young rediae. The facts that small rediae can attack other rediae and concentrate in the anterior parts of the mollusc can be explained by age-related feeding preferences and niche segregation. They are unlikely to be associated with the 'colony' defence against invaders. To sum up, clonal groups of H. elongata rediae in our study represented self-sustaining infrapopulations. We failed to find any arguments in favour of their eusocial organisation.

Caste ratio adjustments in response to perceived and realised competition in parasites with division of labour

“…In addition, investments in defense are not necessarily costly, at least under immediate competition, as shown by the trade‐off between numbers of soldiers and cercarial output only becoming manifest when soldiers become too numerous. It will be interesting to see whether these adaptive responses also occur in other social trematodes, including those where division of labour takes place among age classes of rediae (see Galaktionov et al., ) rather than among distinct castes. More generally, our results provide additional evidence of phenotypic responses to competition in parasites and of state‐dependent strategies in the face of changing and unpredictable conditions (Thomas, Brown, Sukhdeo, & Renaud, ).…”

“…This social organisation into two distinct castes has now been reported in multiple trematode species (Garcia‐Vedrenne et al., , ; Hechinger et al., ; Leung & Poulin, ; Miura, ; Nielsen, Johansen, & Mouritsen, ). In some trematodes, however, the division of labour is age‐based, with young rediae taking on a defensive role and older ones a reproductive function (Galaktionov, Podvyaznaya, Nikolaev, & Levakin, ).…”

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

“…Although the non-reproducing caste might have some other roles (e.g. Lloyd and Poulin, 2012;Galaktionov et al, 2015), it is clear that a major role is defense of colonies (Hechinger et al, 2011;Miura, 2012;Mouritsen and Halvorsen, 2015;Garcia-Vedrenne et al, 2016).…”

Evolution, phylogenetic distribution and functional ecology of division of labour in trematodes

“…In some species, it appears clear that the small soldiers never develop into larger reproductives (see Phenotypic plasticity of caste members below), and that this is a true case of division of labour between two distinct castes. In others, the division of labour may instead be age-structured, with younger and smaller rediae acting as soldiers before they grow into reproductive individuals [11, 12]. In fact, the mere existence of castes and division of labour in trematodes is not without controversy; Galaktionov et al [12] provide an alternative interpretation based on allometric growth from young to older rediae and other age-related differences in mobility and function.…”