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

Abstract

Colonial organisms with division of labour are assumed to achieve increased colony-level efficiency in task performance through functional specialisation of individuals into distinct castes. In social insects, ratios of individuals in different castes can adjust adaptively in response to external threats. However, whether flexibility in caste ratio also occurs in other social organisms with division of labour remains unclear. Some parasitic trematodes, in which clonal colonies within the snail intermediate host comprise a reproductive caste and a soldier caste, offer good systems to test the general nature of adaptive caste ratio adjustments. Using the trematode Philophthalmus sp. as model, we test whether trematode colonies shift their composition towards more soldiers when exposed to a sustained risk of invasion by a competitor parasite species, and/or when experiencing sustained, active competition. We also quantify the colony-level fitness impact of caste ratio adjustments, measured as the colony's output of larval infective stages. We conducted two long-term laboratory experiments on within-snail trematode colonies. First, snails harbouring Philophthalmus colonies were exposed to different levels of invasion risk by another trematode species, Maritrema novaezealandense. Second, the structure of Philophthalmus colonies was quantified after a year-long period of within-snail competition with the other trematode species. When facing the risk of invasion by a competitor, independently of the level of risk, Philophthalmus colonies showed a significant shift towards producing more soldiers, resulting in altered caste ratio. Similarly, when experiencing actual competition by another trematode established in the same snail, Philophthalmus colonies also adjusted by producing significantly more soldiers. Greater investments in defense via more soldiers had negative impacts on the establishment and size of the competitor's colonies. Nevertheless, the presence of the competitor reduced the fitness (output of infective stages) of Philophthalmus colonies, although the production of more soldiers mitigated that effect. Our findings demonstrate that trematode colonies with division of labour are capable of adaptive caste ratio adjustments in response to both the perceived threat of competition and actual competition, with trade-offs against reproductive success only apparent when soldier numbers are very high. Combined with results on social insects, our study suggests parallel adaptations of colonial organisms in phylogenetically disparate organisms.

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

“…These results support earlier findings [39] and are also aligned with findings on different trematode species with division of labour [40]. Caste ratio adjustments appear to be effective at eliminating the competitor: the size of Maritrema colonies (number of sporocysts) is significantly negatively correlated with the number of soldiers in the Philophthalmus colony sharing their snail [34].

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“…These results come from naturally infected snails that were brought to the laboratory with their existing infections. A similar shift in caste ratio was observed in Philophthalmus colonies whose snail host was invaded by Maritrema following experimental exposure to Maritrema eggs, compared to Philophthalmus colonies whose snail host was not invaded [34]. These results support earlier findings [39] and are also aligned with findings on different trematode species with division of labour [40].…”

“…Among these, Maritrema novaezealandense (Microphallidae; hereafter just Maritrema ) is by far the most prevalent, infecting almost half of the snails in some Z. subcarinatus populations and frequently co-infecting the same individual snails as Philophthalmus . The long-term cercarial output of Philophthalmus colonies is reduced by about 50% when they share their snail with Maritrema [33, 34], therefore competition has huge fitness impacts for Philophthalmus .…”

Social trematode parasites increase standing army size in areas of greater invasion threat

“…However, the small number of localities in these studies preclude directly assessing the relationship between soldier allocation and invasion threat. Second, laboratory experiments using social insects and trematodes show that colonies can plastically allocate more to defence [9][10][11]. Despite such tantalizing evidence, we lack research with the replication required to robustly test whether spatial variability in invasion threat matches field patterns of allocation to the soldier caste.…”

“…Theory predicts that these colonies should invest relatively more in the soldier caste in response to increased threat [5,7,8]. Indeed, manipulative experiments show that colonial societies of a wasp, an ant and a trematode species can increase the number of soldiers in response to increased threat [9][10][11].…”