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1. Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode‐amphipod system

   https://doi.org/10.1111/mec.17093  

   Rand, David M. ; Nunez, Joaquin C. B. ; Williams, Shawn ; Rong, Stephen ; Burley, John T. ; Neil, Kimberly B. ; Spierer, Adam N. ; McKerrow, Wilson ; Johnson, David S. ; Raynes, Yevgeniy ; et al ( August 2023 , Molecular Ecology)

   Manipulation of host phenotypes by parasites is hypothesized to be an adaptive strategy enhancing parasite transmission across hosts and generations. Characterizing the molecular mechanisms of manipulation is important to advance our understanding of host–parasite coevolution. The trematode (Levinseniella byrdi) is known to alter the colour and behaviour of its amphipod host (Orchestia grillus) presumably increasing predation of amphipods which enhances trematode transmission through its life cycle. We sampled 24 infected and 24 uninfected amphipods from a salt marsh in Massachusetts to perform differential gene expression analysis. In addition, we constructed novel genomic tools forO. grillusincluding a de novo genome and transcriptome. We discovered that trematode infection results in upregulation of amphipod transcripts associated with pigmentation and detection of external stimuli, and downregulation of multiple amphipod transcripts implicated in invertebrate immune responses, such as vacuolar ATPase genes. We hypothesize that suppression of immune genes and the altered expression of genes associated with coloration and behaviour may allow the trematode to persist in the amphipod and engage in further biochemical manipulation that promotes transmission. The genomic tools and transcriptomic analyses reported provide new opportunities to discover how parasites alter diverse pathways underlying host phenotypic changes in natural populations.

    

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2. The visual ecology of selective predation: Are unhealthy hosts less stealthy hosts?

   https://doi.org/10.1002/ece3.8464  

   Wale, Nina ; Fuller, Rebecca C. ; Johnsen, Sönke ; Turrill, McKenna L. ; Duffy, Meghan. A. ( December 2021 , Ecology and Evolution)

   Predators can strongly influence disease transmission and evolution, particularly when they prey selectively on infected hosts. Although selective predation has been observed in numerous systems, why predators select infected prey remains poorly understood. Here, we use a mathematical model of predator vision to test a long‐standing hypothesis about the mechanistic basis of selective predation in aDaphnia–microparasite system, which serves as a model for the ecology and evolution of infectious diseases. Bluegill sunfish feed selectively onDaphniainfected by a variety of parasites, particularly in water uncolored by dissolved organic carbon. The leading hypothesis for selective predation in this system is that infection‐induced changes in the transparency ofDaphniarender them more visible to bluegill. Rigorously evaluating this hypothesis requires that we quantify the effect of infection on the visibility of prey from the predator's perspective, rather than our own. Using a model of the bluegill visual system, we show that three common parasites,Metschnikowia bicuspidata,Pasteuria ramosa, andSpirobacillus cienkowskii, decrease the transparency ofDaphnia, rendering infectedDaphniadarker against a background of bright downwelling light. As a result of this increased brightness contrast, bluegill can see infectedDaphniaat greater distances than uninfectedDaphnia—between 19% and 33% further, depending on the parasite.PasteuriaandSpirobacillusalso increase the chromatic contrast ofDaphnia. These findings lend support to the hypothesis that selective predation by fish on infectedDaphniacould result from the effects of infection onDaphnia's visibility. However, contrary to expectations, the visibility ofDaphniawas not strongly impacted by water color in our model. Our work demonstrates that models of animal visual systems can be useful in understanding ecological interactions that impact disease transmission.

    

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3. Parasitic manipulation or by-product of infection: an experimental approach using trematode-infected snails

   https://doi.org/10.1017/s0022149x21000699  

   Namias, Alice ; Delph, Lynda F. ; Lively, Curtis M. ( January 2022 , Journal of Helminthology)

   Abstract Natural selection should favour parasite genotypes that manipulate hosts in ways that enhance parasite fitness. However, it is also possible that the effects of infection are not adaptive. Here we experimentally examined the phenotypic effects of infection in a snail–trematode system. These trematodes ( Atriophallophorus winterbourni ) produce larval cysts within the snail's shell ( Potamopyrgus antipodarum ); hence the internal shell volume determines the total number of parasite cysts produced. Infected snails in the field tend to be larger than uninfected snails, suggesting the hypothesis that parasites manipulate host growth so as to increase the space available for trematode reproduction. To test the hypothesis, we exposed juvenile snails to trematode eggs. Snails were then left to grow for about one year in 800-l outdoor mesocosms. We found that uninfected males were smaller than uninfected females (sexual dimorphism). We also found that infection did not affect the shell dimensions of males. However, infected females were smaller than uninfected females. Hence, infection stunts the growth of females, and (contrary to the hypothesis) it results in a smaller internal volume for larval cysts. Finally, infected females resembled males in size and shape, suggesting the possibility that parasitic castration prevents the normal development of females. These results thus indicate that the parasite is not manipulating the growth of infected hosts so as to increase the number of larval cysts, although alternative adaptive explanations are possible. 

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4. Infectivity of the parasite Metschnikowia bicuspidata is decreased by time spent as a transmission spore, but exposure to phycotoxins in the water column has no effect

   https://doi.org/10.1111/fwb.14082  

   Sánchez, Kristel F. ; Zhong, Baili ; Agudelo, Jorge A. ; Duffy, Meghan A. ( April 2023 , Freshwater Biology)

   Transmission from one host to another is a crucial component of parasite fitness. For some aquatic parasites, transmission occurs via a free‐living stage that spends time in the water, awaiting an encounter with a new host. These parasite transmission stages can be impacted by biotic and abiotic factors that influence the parasite's ability to successfully infect or grow in a new host.

   Here we tested whether time spent in the water column and/or exposure to common cyanobacterial toxins impacted parasite transmission stages. More specifically, we tested whether the infectivity, within host growth, and virulence of the fungal parasiteMetschnikowia bicuspidatachanged as a result of time spent in the water or from exposure to cyanotoxins in the water column. We exposed parasite transmission spores to different levels of one of two ecologically important cyanotoxins, microcystin‐LR and anatoxin‐a, and factorially manipulated the amount of time spores were incubated in water. We removed the toxins and used those same spores to infect one genotype of the common lake zooplanktonDaphnia dentifera.

   We found that cyanotoxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, we found that spending longer as a transmission spore decreased a spore's chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts.

   We also found a negative relationship between the final spore yield from infected hosts and the proportion of hosts that became infected. In treatments where spores spent longer in the water column prior to encountering a host, infection prevalence was lower (indicating lower per spore infectivity), but each infected host yielded more spores at the end of infection. We hypothesise that this pattern may result from intraspecific parasite competition within the host.

   Overall, these results suggest that transmission spores of this parasite are not strongly influenced by cyanotoxins in the water column, but that other aspects of spending time in the water strongly influence parasite fitness.

    

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5. Transcriptomics of monarch butterflies ( Danaus plexippus ) reveals that toxic host plants alter expression of detoxification genes and down‐regulate a small number of immune genes

   https://doi.org/10.1111/mec.15219  

   Tan, Wen‐Hao ; Acevedo, Tarik ; Harris, Erica V. ; Alcaide, Tiffanie Y. ; Walters, James R. ; Hunter, Mark D. ; Gerardo, Nicole M. ; de Roode, Jacobus C. ( September 2019 , Molecular Ecology)

   Herbivorous insects have evolved many mechanisms to overcome plant chemical defences, including detoxification and sequestration. Herbivores may also use toxic plants to reduce parasite infection. Plant toxins could directly interfere with parasites or could enhance endogenous immunity. Alternatively, plant toxins could favour down‐regulation of endogenous immunity by providing an alternative (exogenous) defence against parasitism. However, studies on genomewide transcriptomic responses to plant defences and the interplay between plant toxicity and parasite infection remain rare. Monarch butterflies (Danaus plexippus) are specialist herbivores of milkweeds (Asclepiasspp.), which contain toxic cardenolides. Monarchs have adapted to cardenolides through multiple resistance mechanisms and can sequester cardenolides to defend against bird predators. In addition, high‐cardenolide milkweeds confer monarch resistance to a specialist protozoan parasite (Ophryocystis elektroscirrha). We used this system to study the interplay between the effects of plant toxicity and parasite infection on global gene expression. We compared transcriptional profiles between parasite‐infected and uninfected monarch larvae reared on two milkweed species. Our results demonstrate that monarch differentially express several hundred genes when feeding onA. curassavicaandA. incarnata, two species that differ substantially in cardenolide concentrations. These differentially expressed genes include genes within multiple families of canonical insect detoxification genes, suggesting that they play a role in monarch toxin resistance and sequestration. Interestingly, we found little transcriptional response to infection. However, parasite growth was reduced in monarchs reared onA. curassavica, and in these monarchs, several immune genes were down‐regulated, consistent with the hypothesis that medicinal plants can reduce reliance on endogenous immunity.

    

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