Caste formation in larval Himasthla elongata (Trematoda) infecting common periwinkles Littorina littorea

Abstract

Reproductive division of labour is well-known in several animal groups but the ecological factors driving the evolution of such social organization are still being discussed. Recent studies have discovered social organization in four marine species of trematode parasites having two distinct castes specialized for reproduction and defence of the clonal intra-molluscan larval colony, respectively. Here, we provide novel evidence for social structure also in colonies of the trematode Himasthla elongata infecting the common periwinkle Littorina littorea. We found two types of rediae, the parthenogenetic larval offspring of the parasite: small non-reproductive rediae and considerably larger reproductive rediae. Both redial types possessed a digestive system, collar and posterior appendages and, hence, aside from dimensions, were morphologically similar. However, in vitro experiments showed that non-reproductive morphs attacked heterospecific competing parasites at a higher rate (2–3 fold) than reproductive morphs did. No within-colony antagonism was observed. In contrast to a previous study on a congeneric trematode species, our findings suggest a relatively weak caste formation in H. elongata, possibly resulting from a corresponding weaker level of interspecific competition.

Social flatworms: the minor caste is adapted for attacking competing parasites

“…(1) Cohortes and thus well-defined multimodal size-frequency distributions are common in agestructured populations of also non-social organisms, and hence, separated redial size groups are no proof of physical caste formation. Moreover, intermediate sizes do exist in the studied trematode species (Hechinger et al 2011;Leung and Poulin 2011;Miura 2012;Nielsen et al 2014). …”

“…Aside from being able to feed directly on host tissues, the redial stage also allows for antagonistic behaviour directed towards competitors that can be seized and eaten (Sousa 1993;Kuris and Lafferty 1994;Galaktionov and Dobrovolskij 2003). Across the studied trematode systems (Hechinger et al 2011;Leung and Poulin 2011;Lloyd and Poulin 2012;Miura 2012;Nielsen et al 2014), several lines of evidence have been provided in support of physical and functional caste formation in the redial colonies. (1) The colonies show bimodal size-frequency distributions with few intermediate sizes.…”

“…(2) As opposed to social arthropods possessing hardened exoskeleton, the body of parasitic flatworms is extremely flexible, and when containing late-stage progeny, it can be considerably enlarged (Hechinger et al 2011;Nielsen et al 2014). Hence, a greater feeding apparatus-to-body size ratio seen in non-reproductive compared with reproductive rediae does not necessarily reflect functional adaptation (i.e.…”

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

“…The nature of this turnover is species-specific (see Introduction) and may be determined both by host-related factors (such as the physiological state and size) and environmental ones (such as the temperature). This explains the differences in the proportion of different redial types in snails of approximately the same size (this study) and in snails of different sizes (Leung and Poulin 2011, Zikmundová 2011, Nielsen et al 2014) collected in localities (Nielsen et al 2014) and geographical regions (Lloyd and Poulin 2014) with differing environmental parameters.…”

“…Large reproductives are considerably less active. They do not attack hetero-or conspecifics or do so much more rarely and slowly (Hechinger et al 2011, Leung and Poulin 2011, Nielsen et al 2014.…”