Parasite-Modified Chemical Communication: Implications for Aquatic Community Dynamics

Friesen, Olwyn C.; Detwiler, Jillian T.

doi:10.3389/fevo.2021.634754

Cited by 7 publications

(10 citation statements)

References 89 publications

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“…For host density to affect haemocyte production and other measures of immune defences, snails must recognize that they are aggregating. In higher densities, snails could communicate by physical or chemical cues though our experiments focused on chemical communication because a number of studies have suggested that snails communicate through signaling molecules in snail-conditioned water (55,(79)(80)(81). We characterized fatty acids from snail water because several of them are the biosynthetic precursors of compounds that function in the immune defences of invertebrates and vertebrates (46,82).…”

Section: Discussionmentioning

confidence: 99%

“…There is an evolutionary benefit for a snail to respond prophylactically via cues from signaling molecules that more specifically indicate whether the risk is from a pathogen or parasite. However, much more research is needed to further understand the generality and strength of alterations to oxylipins in response to infection, how these may vary with host and parasite diversity, and how these changes may impact density-dependent prophylaxis ( 55 ). Further, studies on additional invertebrates are needed to understand the evolution of DDP and determine whether similar mechanisms are used across taxa.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, tests for DDP in nature should quantify infection risk by assessing first intermediate host prevalence and density, and then determine whether co-occurring second intermediate hosts have lower metacercarial infections due to increased investment in their immune systems. In addition to studying this phenomenon in natural populations, future laboratory experiments should explore how oxylipin signals may be detected through the signaling web found within aquatic communities ( 55 ). The impacts of these modified chemical cues on the behaviour of other community members, such as other invertebrates and fish, are yet to be fully explored ( 55 ).…”

Section: Discussionmentioning

confidence: 99%

“…Oxylipins influence many functional aspects of an organism's biology. In molluscs, oxylipins affect the neuro-and reproductive physiology and their interactions with parasites (42,46,50,(52)(53)(54)(55). Intriguingly, oxylipins are not just produced by free-living organisms.…”

Section: Introductionmentioning

confidence: 99%

“…Some parasites, including the human trematode Schistosoma mansoni , synthesize oxylipins that play a role in parasite development, penetration of the host, and modulating host defences ( 46 , 56 – 58 ). However, considering the diversity of invertebrate hosts and their parasites, the function and ecological role of oxylipins is largely unknown ( 55 , 57 , 58 ). To our knowledge, the function of oxylipins in snail host aggregation behaviour and DDP has yet to be determined.…”

Section: Introductionmentioning

confidence: 99%

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Density-Dependent Prophylaxis in Freshwater Snails Driven by Oxylipin Chemical Cues

Friesen

Sykes

et al. 2022

Front. Immunol.

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While animal aggregations can benefit the fitness of group members, the behaviour may also lead to higher risks of parasite infection as group density increases. Some animals are known to moderate their investment in immunity relative to the risk of infection. These animals exhibit density-dependent prophylaxis (DDP) by increasing their immune investment as group density increases. Despite being documented in many taxa, the mechanisms of DDP remain largely unexplored. Snails are known to aggregate and experience large fluctuations in density and serve as required hosts for many parasites. Further, they are known to use chemical cues to aggregate. To test whether freshwater snails exhibit DDP and investigate the role that chemical signaling compounds may play in triggering this phenomenon, we performed four experiments on the freshwater snail Stagnicola elodes, which is a common host for many trematode parasite species. First, we tested if DDP occurred in snails in laboratory-controlled conditions (control vs snail-conditioned water) and whether differences in exposure to chemical cues affected immune function. Second, we used gas chromatography to characterize fatty acids expressed in snail-conditioned water to determine if precursors for particular signaling molecules, such as oxylipins, were being produced by snails. Third, we characterized the oxylipins released by infected and uninfected field-collected snails, to better understand how differences in oxylipin cocktails may play a role in inducing DDP. Finally, we tested the immune response of snails exposed to four oxylipins to test the ability of specific oxylipins to affect DDP. We found that snails exposed to water with higher densities of snails and raised in snail-conditioned water had higher counts of haemocytes. Additionally, lipid analysis demonstrated that fatty acid molecules that are also precursors for oxylipins were present in snail-conditioned water. Trematode-infected snails emitted 50 oxylipins in higher amounts, with 24 of these oxylipins only detected in this group. Finally, oxylipins that were higher in infected snails induced naïve snails to increase their immune responses compared to sham-exposed snails. Our results provide evidence that snails exhibit DDP, and the changes in oxylipins emitted by infected hosts may be one of the molecular mechanisms driving this phenomenon.

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