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

Author:

Rand David M.123ORCID,Nunez Joaquin C. B.1,Williams Shawn12,Rong Stephen13,Burley John T.14,Neil Kimberly B.1,Spierer Adam N.1,McKerrow Wilson5,Johnson David S.6,Raynes Yevgeniy1,Fayton Thomas J.78,Skvir Nicholas2,Ferranti David A.1,Zeff Maya Greenhill1ORCID,Lyons Amanda1,Okami Naima1,Morgan David M.1,Kinney Kealohanuiopuna9,Brown Bianca R. P.14,Giblin Anne E.10,Cardon Zoe G.10

Affiliation:

1. Department of Ecology, Evolution and Organismal Biology Brown University Providence Rhode Island USA

2. Department of Molecular Biology, Cell Biology, and Biochemistry Brown University Providence Rhode Island USA

3. Center for Computational Molecular Biology Brown University Providence Rhode Island USA

4. Institute at Brown for Environment and Society Brown University Providence Rhode Island USA

5. Division of Applied Mathematics Brown University Providence Rhode Island USA

6. Department of Biological Sciences Virginia Institute of Marine Science, William & Mary Gloucester Point Virginia USA

7. University of Southern Mississippi Hattiesburg Mississippi USA

8. Cornell University Ithaca New York USA

9. US Forest Service Hilo Hawaii USA

10. Ecosystems Center Marine Biological Laboratory Woods Hole Massachusetts USA

Abstract

AbstractManipulation 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.

Funder

National Institutes of Health

National Science Foundation

Publisher

Wiley

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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