Save your host, save yourself? Caste‐ratio adjustment in a parasite with division of labor and snail host survival following shell damage

Abstract

Shell damage and parasitic infections are frequent in gastropods, influencing key snail host life‐history traits such as survival, growth, and reproduction. However, their interactions and potential effects on hosts and parasites have never been tested. Host–parasite interactions are particularly interesting in the context of the recently discovered division of labor in trematodes infecting marine snails. Some species have colonies consisting of two different castes present at varying ratios; reproductive members and nonreproductive soldiers specialized in defending the colony. We assessed snail host survival, growth, and shell regeneration in interaction with infections by two trematode species, Philophthalmus sp. and Maritrema novaezealandense, following damage to the shell in the New Zealand mud snail Zeacumantus subcarinatus. We concomitantly assessed caste‐ratio adjustment between nonreproductive soldiers and reproductive members in colonies of the trematode Philophthalmus sp. in response to interspecific competition and shell damage to its snail host. Shell damage, but not parasitic infection, significantly increased snail mortality, likely due to secondary infections by pathogens. However, trematode infection and shell damage did not negatively affect shell regeneration or growth in Z. subcarinatus; infected snails actually produced more new shell than their uninfected counterparts. Both interspecific competition and shell damage to the snail host induced caste‐ratio adjustment in Philophthalmus sp. colonies. The proportion of nonreproductive soldiers increased in response to interspecific competition and host shell damage, likely to defend the parasite colony and potentially the snail host against increasing threats. These results indicate that secondary infections by pathogens following shell damage to snails both significantly increased snail mortality and induced caste‐ratio adjustments in parasites. This is the first evidence that parasites with a division of labor may be able to produce nonreproductive soldiers according to environmental factors other than interspecific competition with other parasites.

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

“…After 7 months of biweekly exposure to bird faeces and potential infection by a competitor, snail survival was high and generally similar among the eight experimental combinations (i.e., Philophthalmus ‐infected vs. Philophthalmus ‐free snails; zero, low, medium and high exposure levels to Maritrema ), ranging between 81% and 96%. As observed in previous studies, survival was slightly higher in Philophthalmus ‐infected (93%) than Philophthalmus ‐free snails (85%; Fisher's exact test, χ² = 16.15, p = 0.0001; see Fredensborg, Mouritsen, & Poulin, ; Lloyd & Poulin, ; MacLeod, Poulin, & Lagrue, ). However, no difference was detected among the three exposure levels (Fisher's exact tests, all p > 0.05).…”

Environmental determinants of distribution of freshwater snails and trematode infection in the Omo Gibe River Basin, southwest Ethiopia

“…Overall, snails harbouring co-infections were found less frequently in the study area, indicating that antagonistic interactions may be occurring between different trematodes within the snail, limiting or excluding the establishment of some species [31, 32]. The intensity of co-infecting trematodes is governed by rediae through their antagonistic interspecific interactions against other parasites attempting to infect the same snail host [33, 34]. This is consistent with the fact that interspecific competition for resources and space represents a potentially strong selection pressure for trematodes infecting snail hosts [11].…”

Stable isotopes unravel the feeding mode–trophic position relationship in trematode parasites

“…Philophthalmus attenuatus utilises two distinct forms of rediae, a small size class that plays a defensive role and a large size class that plays a reproductive role (Hechinger et al, 2011;Leung & Poulin, 2011), both of which possess rudimentary mouth parts and digestive organs. The small size class, often referred to as a soldier caste, has been shown to attack/consume competitor parasites within the same snail host (Lagrue et al, 2018) and may also play a role in the removal/consumption of fungal or bacterial pathogens (MacLeod et al, 2018). This more aggressive size class may alter the intake of nutrients such that δ 15 N values are elevated relative to trematode species that use only a single size class of rediae, one that is assumed to have to play both defensive and reproductive roles (Sousa, 1983).…”