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

Abstract

Division of labour has evolved in many social animals where colonies consist of clones or close kin. It involves the performance of different tasks by morphologically distinct castes, leading to increased colony fitness. Recently, a form of division of labour has been discovered in trematodes: clonal rediae inside the snail intermediate host belong either to a large-bodied reproductive caste, or to a much smaller and morphologically distinct ‘soldier’ caste which defends the colony against co-infecting trematodes. We review recent research on this phenomenon, focusing on its phylogenetic distribution, its possible evolutionary origins, and how division of labour functions to allow trematode colonies within their snail host to adjust to threats and changing conditions. To date, division of labour has been documented in 15 species from three families: Himasthlidae, Philophthalmidae and Heterophyidae. Although this list of species is certainly incomplete, the evidence suggests that division of labour has arisen independently more than once in the evolutionary history of trematodes. We propose a simple scenario for the gradual evolution of division of labour in trematodes facing a high risk of competition in a long-lived snail host. Starting with initial conditions prior to the origin of castes (size variation among rediae within a colony, size-dependent production of cercariae by rediae, and a trade-off between cercarial production and other functions, such as defence), maximising colony fitness (R0) can lead to caste formation or the age-structured division of labour observed in some trematodes. Finally, we summarise recent research showing that caste ratios, i.e. relative numbers of reproductive and soldier rediae per colony, become more soldier-biased in colonies exposed to competition from another trematode species sharing the same snail, and also respond to other stressors threatening the host’s survival or the colony itself. In addition, there is evidence of asymmetrical phenotypic plasticity among individual caste members: reproductives can assume defensive functions against competitors in the absence of soldiers, whereas soldiers are incapable of growing into reproductives if the latter’s numbers are reduced. We conclude by highlighting future research directions, and the advantages of trematodes as model systems to study social evolution.

Clonemate cotransmission supports a role for kin selection in a puppeteer parasite

“…The obligate asexual reproductive stage of D. dendriticum in its snail first host has enabled the highest degree of genetic relatedness: i.e., clonality. Given the ubiquity of obligate asexual reproduction among digeneans, it will be of interest to quantify clonemates and explore the role of kin selection in the evolution of other trematode traits: e.g., larval-stage division of labor within mollusc hosts (61,62) or competition outcomes for coinfecting metacercariae (e.g., ref. 63).…”

The weird eusociality of polyembryonic parasites

“…Recently, however, larval colonies of trematodes (i.e. flatworms, blood flukes) are argued to be eusocial, following the discovery of morphologically distinct soldier castes [7], and this claim has received growing support [8][9][10][11][12][13]. This discovery is unexpected and exciting, extending our social evolutionary theories into a phylum (Platyhelminthes) that seemingly had no relevance to social evolution research.…”

Cost of interspecific competition between trematode colonies

“…During the last decade, a range of trematode species originating from three different families have been shown to have their intramolluscan redial colonies divided into two morphologically and functionally distinct groups or castes (Poulin et al ., 2019). The minor caste (soldiers) is primarily engaged in defending the colony against other invading parasites, whereas the considerably larger colony members are mostly engaged in producing the colony's cercarial dispersal stages (the reproductive caste).…”

“…If such a predatory role by the smaller parthenitae is, indeed, an adaptation resulting from natural selection under competitive pressures from co-infecting parasite species (see Poulin et al ., 2019), it requires that the fitness of trematode colonies is negatively affected by co-infections. Surprisingly, this important evolutionary premise has been scrutinized in only two of the 15 socially organized systems so far identified, and demonstrated in just one of them.…”

“…As stressed by Poulin et al . (2019), other fitness components can be evolutionary targeted – for instance, the duration of infection rather than the parasite's immediate reproductive rate during competition events (i.e. lifetime rather than short-term reproductive success).…”