Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode-amphipod system

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Date
2023-08-04
Authors
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
Fayton, Thomas J.
Skvir, Nicholas
Ferranti, David A.
Zeff, Maya Greenhill
Lyons, Amanda
Okami, Naima
Morgan, David M.
Kinney, Kealohanuiopuna
Brown, Bianca R. P.
Giblin, Anne E.
Cardon, Zoe G.
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10.1111/mec.17093
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Keywords
Amphipod
Differential expression
Ecological genomics
Host–parasite co-evolution
Infection response
Orchestia grillus
Parasite manipulation
Population genetics
Trematode
Abstract
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 for O. grillus including 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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© The Author(s), 2023. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Rand, D., Nunez, J., Williams, S., Rong, S., Burley, J., Neil, K., Spierer, A., McKerrow, W., Johnson, D., Raynes, Y., Fayton, T., Skvir, N., Ferranti, D., Zeff, M., Lyons, A., Okami, N., Morgan, D., Kinney, K., Brown, B., Giblin, A., & Cardon, Z. (2023). Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode‐amphipod system. Molecular Ecology, https://doi.org/10.1111/mec.17093.
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Rand, D., Nunez, J., Williams, S., Rong, S., Burley, J., Neil, K., Spierer, A., McKerrow, W., Johnson, D., Raynes, Y., Fayton, T., Skvir, N., Ferranti, D., Zeff, M., Lyons, A., Okami, N., Morgan, D., Kinney, K., Brown, B., Giblin, A., & Cardon, Z. (2023). Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode‐amphipod system. Molecular Ecology.
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