Host preference of field‐derived Schistosoma mansoni is influenced by snail host compatibility and infection status

Abstract

Schistosome parasites cause a chronic inflammatory disease in humans, and recent studies have emphasized the importance of control programs for understanding the aquatic phases of schistosomiasis transmission. The host-seeking behavior of larval schistosomes (miracidia) for their snail intermediate hosts plays a critical role in parasite transmission. Using field-derived strains of Kenyan snails and parasites, we tested two main hypotheses: (1) Parasites prefer the most compatible host, and (2) parasites avoid hosts that are already infected. We tested preference to three Biomphalaria host snail taxa (B. pfeifferi, B. sudanica, and B. choanomphala), using allopatric and sympatric Schistosoma mansoni isolates and two different nonhost snail species that cooccur with Biomphalaria, Bulinus globosus, and Physa acuta. We also tested whether schistosomes avoid snail hosts that are already infected by another trematode species and whether competitive dominance played a role in their behavior. Preference was assessed using two-way choice chambers and by visually counting parasites that moved toward competing stimuli. In pairwise comparisons, we found that S. mansoni did not always prefer the more compatible snail taxon, but never favored an incompatible host over a compatible host. While parasites preferred B. pfeifferi to the nonhost species B. globosus, they did not significantly prefer B. pfeifferi versus P. acuta, an introduced species in Kenya. Finally, we demonstrated that parasites avoid infected snails if the resident parasite was competitively dominant (Patagifer sp.), and preferred snails infected with subordinates (xiphidiocercariae) to uninfected snails. These results provide evidence of "fine tuning" in the ability of schistosome miracidia to detect hosts; however, they did not always select hosts that would maximize fitness. Appreciating such discriminatory abilities could lead to a better understanding of how ecosystem host and parasite diversity influences

Helminth-host-environment interactions: Looking down from the tip of the iceberg

“…This latter observation is consistent with the nutritional and reproductive benefit that E. caproni gains from infecting an S. mansoni -infected snail (Carpenter et al 2021). A follow-up study (Laidemitt et al 2022) extended these findings by showing that miracidia avoided snails infected with the dominant competitor Patigifer but moved toward snails infected with a subordinate xiphiodiocercarial infection or with the metacerarcial stage of Patagifer.…”

Coinfection accelerates transmission to new hosts despite no effects on virulence and parasite growth

“…How such direct measures of transmission, independent of within-host processes (e.g. virulence), actually scale up and affect the spread of T. urticae across a population of potential hosts is not straightforward and may well depend on the presence and relative densities of interspecific competitors [20]. Moreover, different life-history strategies could co-exist in a parasite population, some maximizing fitness within hosts and others maximizing the spread across hosts.…”

“…Interactions among parasites may also impact transmission-related traits independently of growth and virulence, such as triggering dispersal from hosts infected with competitors or impacting whether a new host becomes infected. Indeed, certain parasites avoid or choose a host, or a host tissue, depending on its infection status [20,21]. This means that multiple parasites in the environment have the potential to impact parasite life-history ecology and evolution at different scales, not restricted to the within-host environment.…”

Snail hosts abundance mediates the effects of antagonist interactions between trematodes on the transmission of human schistosomes.

“…However, coinfection rates observed in natura are generally lower than this theoretical expectation. Interspecific competition leading to the rapid exclusion of one interacting species, recruitment heterogeneity either due to random or parasite behaviours that limit co-infections, immune priming mechanisms and high cost of co-infection on hosts fitness, may explain the departure of this theoretical expectation as generally observed in natura (15,16). Intriguingly, the effect of host abundance on co-infection rates is generally neglected since this theoretical expectation relies on the relative prevalence of co-infection, which corresponds to the proportion of hosts that are infected (or co-infected) among all hosts present in the environment.…”