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Variable host responses mediate host preference in marine flatworm-snail symbioses.

ABSTRACT: Host preference of symbionts evolves from fitness trade-offs. However, it is often unclear how interspecific variations in host response traits influence this evolutionary process. Using the association between the polyclad flatworm Paraprostatum echinolittorinae and its intertidal snail hosts on the Pacific Coast of Panama, we assessed how a symbiont's host preference is associated with varying host defenses and post-infestation performances. We first characterized the prevalence and intensity of worm infestation in five snail hosts (Tegula pellisserpentis, Nerita scabricosta, N. funiculata, Planaxis planicostatus, and Cerithium stercusmuscarum). We then used manipulative experiments to test flatworm's host choice, hosts' behavioral rejection of flatworms, and hosts' growth and survival following the infestation. In the field, flatworms were orders of magnitude more prevalent and dense in T. pellisserpentis, N. scabricosta, N. funiculata than P. planicostatus and C. stercusmuscarum, although the three former hosts were not necessarily more abundant. The results from our laboratory host selection trials mirrored these patterns; flatworms were 3 to 14 times more likely to choose T. pellisserpentis, N. scabricosta, N. funiculata over P. planicostatus and C. stercusmuscarum. The less preferred hosts frequently rejected flatworms via mantle contractions and foot withdrawals, which reduced the infestation rate by 39%-67%. These behaviors were less frequent or absent in the preferred hosts. Flatworm infestation variably influenced host performances in the field, negligibly affecting the growth and survival of T. pellisserpentis and N. funiculata but reducing the growth of P. planicostatus. Flatworms thus preferred less defended hosts that can also support higher worm densities without being harmed. Stable isotope analysis further revealed that flatworms are unlikely to feed on snail tissues and may live as a commensal in their preferred hosts. Our study demonstrates that host response traits can modulate a symbiont's host choice and calls for more explicit considerations of host response variability in host preference research.

SUBMITTER: Lee J

PROVIDER: S-EPMC7924752 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Variable host responses mediate host preference in marine flatworm-snail symbioses.

Lee Juhyung J Davidson Timothy M TM Torchin Mark E ME

PloS one 20210302 3

Host preference of symbionts evolves from fitness trade-offs. However, it is often unclear how interspecific variations in host response traits influence this evolutionary process. Using the association between the polyclad flatworm Paraprostatum echinolittorinae and its intertidal snail hosts on the Pacific Coast of Panama, we assessed how a symbiont's host preference is associated with varying host defenses and post-infestation performances. We first characterized the prevalence and intensity ...[more]

PMID: 33651807

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Project description: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 co-occur 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 disease transmission and could provide novel control mechanisms to improve human health.

Dataset Information

Variable host responses mediate host preference in marine flatworm-snail symbioses.

Publications

Variable host responses mediate host preference in marine flatworm-snail symbioses.

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