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Two parasites in one host: spatiotemporal dynamics and co-occurrence of Microsporidia and Rickettsia in an amphipod host

Published online by Cambridge University Press:  24 May 2021

Eunji Park Open the ORCID record for Eunji Park [Opens in a new window]  and
Robert Poulin Open the ORCID record for Robert Poulin [Opens in a new window]
Eunji Park*
Affiliation:
Department of Zoology, University of Otago, 340 Great King Street, Dunedin 9016, New Zealand
Robert Poulin
Affiliation:
Department of Zoology, University of Otago, 340 Great King Street, Dunedin 9016, New Zealand
*
Author for correspondence: Eunji Park, E-mail: [email protected]
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Abstract

Biological interactions can greatly influence the abundance of species. This is also true for parasitic species that share the same host. Microsporidia and Rickettsia are widespread intracellular parasites in populations of Paracalliope fluviatilis, the most common freshwater amphipods in New Zealand. Although both parasites coexist in many populations, it is unclear whether they interact with each other. Here, we investigated spatial−temporal dynamics and co-occurrence of the two parasites, Microsporidia and Rickettsia in P. fluviatilis hosts, across one annual cycle and in three different locations. Prevalence of both Microsporidia and Rickettsia changed over time. However, while the prevalence of Rickettsia varied significantly between sampling times, that of Microsporidia did not change significantly and remained relatively low. The two parasites therefore followed different temporal patterns. Also, the prevalence of both parasites differed among locations, though the two species reached their highest prevalence in different locations. Lastly, there was no evidence for positive or negative associations between the two parasite species; the presence of one parasite in an individual host does not appear to influence the probability of infection by the other parasite. Their respective prevalence may follow different patterns among populations on a larger spatial scale due to environmental heterogeneity across locations.

Keywords

Coinfectionintracellular parasitesmultiple infectionsseasonalitywithin-host competition
Type
Research Article
Information
Parasitology , Volume 148 , Issue 9 , August 2021 , pp. 1099 - 1106
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Altizer, S, Dobson, A, Hosseini, P, Hudson, P, Pascual, M and Rohani, P (2006) Seasonality and the dynamics of infectious diseases. Ecology letters 9, 467–484CrossRefGoogle ScholarPubMed
Anderson, TK and Sukhdeo, MVK (2010) Abiotic versus biotic hierarchies in the assembly of parasite populations. Parasitology 137, 743–754.CrossRefGoogle ScholarPubMed
Arditi, R and Ginzburg, LR (1989) Coupling in predator-prey dynamics: ratio-dependence. Journal of Theoretical Biology 139, 311–326.CrossRefGoogle Scholar
Arneberg, P, Skorping, A, Grenfell, B and Read, AF (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B: Biological Sciences 265, 1283–1289.CrossRefGoogle Scholar
Arundell, K, Dunn, A, Alexander, J, Shearman, R, Archer, N and Ironside, JE (2015) Enemy release and genetic founder effects in invasive killer shrimp populations of Great Britain. Biological Invasions 17, 1439–1451.CrossRefGoogle Scholar
Asochakov, IA (1994) Technique for measuring body length of amphipods. Hydrobiological Journal 30, 107–110.Google Scholar
Bacela-Spychalska, K, Wróblewski, P, Mamos, T, Grabowski, M, Rigaud, T, Wattier, R, Rewicz, T, Konopacka, A and Ovcharenko, M (2018) Europe-wide reassessment of Dictyocoela (Microsporidia) infecting native and invasive amphipods (Crustacea): molecular versus ultrastructural traits. Scientific Reports 8, 1–16.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, BM and Walker, SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bethel, WM and Holmes, JC (1977) Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.CrossRefGoogle ScholarPubMed
Bojko, J and Ovcharenko, M (2019) Pathogens and other symbionts of the Amphipoda: taxonomic diversity and pathological significance. Diseases of Aquatic Organisms 136, 3–36.CrossRefGoogle ScholarPubMed
Dean, P, Hirt, RP and Embley, TM (2016) Microsporidia: why make nucleotides if you can steal them? PLoS Pathogens 12, e1005870.CrossRefGoogle Scholar
Dezfuli, BS, Giari, L and Poulin, R (2000) Species associations among larval helminths in an amphipod intermediate host. International Journal for Parasitology 30, 1143–1146.CrossRefGoogle Scholar
Dunn, AM and Smith, JE (2001) Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381–388.CrossRefGoogle ScholarPubMed
Dunn, AM, Terry, RS and Smith, JE (2001) Transovarial transmission in the microsporidia. Advances in Parasitology 48, 57–100.CrossRefGoogle ScholarPubMed
Friesen, OC, Goellner, S, Poulin, R and Lagrue, C (2019) Parasites shape community structure and dynamics in freshwater crustaceans. Parasitology 147, 182–193.CrossRefGoogle ScholarPubMed
Grassly, NC and Fraser, C (2006) Seasonal infectious disease epidemiology. Proceedings of the Royal Society B: Biological Sciences 273, 2541–2550.CrossRefGoogle ScholarPubMed
Haine, ER, Boucansaud, K and Rigaud, T (2005) Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society B: Biological Sciences 272, 2505–2510.CrossRefGoogle ScholarPubMed
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.CrossRefGoogle ScholarPubMed
Kikuchi, Y and Fukatsu, T (2005) Rickettsia infection in natural leech populations. Microbial Ecology 49, 265–271.CrossRefGoogle ScholarPubMed
Küchler, SM, Kehl, S and Dettner, K (2009) Characterization and localization of Rickettsia sp. in water beetles of genus Deronectes (Coleoptera: Dytiscidae). FEMS Microbiology Ecology 68, 201–211.CrossRefGoogle Scholar
Lagrue, C, Joannes, A, Poulin, R and Blasco-Costa, I (2016) Genetic structure and host-parasite co-divergence: evidence for trait-specific local adaptation. Biological Journal of the Linnean Society 118, 344–358.CrossRefGoogle Scholar
Lass, S and Ebert, D (2006) Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proceedings of the Royal Society B: Biological Sciences 273, 199–206.CrossRefGoogle ScholarPubMed
Lievens, EJP, Rode, NO, Landes, J, Segard, A, Jabbour-Zahab, R, Michalakis, Y and Lenormand, T (2019) Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (Microsporidia) community. International Journal for Parasitology 49, 471–480.CrossRefGoogle Scholar
Martins, AS and Haimovici, M (1997) Distribution, abundance and biological interactions of the cutlassfish Trichiurus lepturus in the southern Brazil subtropical convergence ecosystem. Fisheries Research 30, 217–227.CrossRefGoogle Scholar
Ovcharenko, MO, Bacela, K, Wilkinson, T, Ironside, JE, Rigaud, T and Wattier, RA (2010) Cucumispora dikerogammari n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers. Parasitology 137, 191–204.CrossRefGoogle ScholarPubMed
Park, E and Poulin, R (2020) Widespread Torix Rickettsia in New Zealand amphipods and the use of blocking primers to rescue host COI sequences. Scientific Reports 10, 16842.CrossRefGoogle ScholarPubMed
Park, E and Poulin, R (2021) Revisiting the phylogeny of Microsporidia. International Journal for Parasitology. In press. doi: 10.1016/j.ijpara.2021.02.005.CrossRefGoogle ScholarPubMed
Park, E, Jorge, F and Poulin, R (2020) Shared geographic histories and dispersal contribute to congruent phylogenies between amphipods and their microsporidian parasites at regional and global scales. Molecular Ecology 29, 3330–3345.CrossRefGoogle ScholarPubMed
Pickup, J and Ironside, JE (2018) Multiple origins of parasitic feminization: thelygeny and intersexuality in beach-hoppers are caused by paramyxid parasites, not microsporidia. Parasitology 145, 408–415.CrossRefGoogle Scholar
Pilgrim, J, Ander, M, Garros, C, Baylis, M, Hurst, GDD and Siozios, S (2017) Torix group Rickettsia are widespread in Culicoides biting midges (Diptera: Ceratopogonidae), reach high frequency and carry unique genomic features. Environmental Microbiology 19, 4238–4255.CrossRefGoogle Scholar
Pollard, W, Omelon, C, Andersen, D and McKay, C (1999) Perennial spring occurrence in the Expedition Fiord area of western Axel Heiberg Island, Canadian high Arctic. Canadian Journal of Earth Sciences 36, 105–120.CrossRefGoogle Scholar
Poulin, R (1999) The intra- and interspecific relationships between abundance and distribution in helminth parasites of birds. Journal of Animal Ecology 68, 719–725.CrossRefGoogle Scholar
Poulin, R (2011) Evolutionary Ecology of Parasites. New Jersey: Princeton University Press. doi: 10.2307/3285737.CrossRefGoogle Scholar
Poulin, R (2020) Meta-analysis of seasonal dynamics of parasite infections in aquatic ecosystems. International Journal for Parasitology 50, 501–510.CrossRefGoogle ScholarPubMed
Poulin, R and Latham, ADM (2002) Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda: Talitridae). Animal Behaviour 63, 269–275.CrossRefGoogle Scholar
Quiles, A, Wattier, RA, Bacela-Spychalska, K, Grabowski, M and Rigaud, T (2020) Dictyocoela microsporidia diversity and co-diversification with their host, a gammarid species complex (Crustacea, Amphipoda) with an old history of divergence and high endemic diversity. BMC Evolutionary Biology 20, 1–17.CrossRefGoogle ScholarPubMed
R Core Team, (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Reddy, AK, Balne, PK, Garg, P and Krishnaiah, S (2011) Is microsporidial keratitis a seasonal infection in India? Clinical Microbiology and Infection 17, 1114–1116.CrossRefGoogle ScholarPubMed
Rigaud, T, Perrot-Minnot, M and Brown, M (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B: Biological Sciences 277, 3693–3702.CrossRefGoogle ScholarPubMed
Robertson, DR (1996) Interspecific competition controls abundance and habitat use of territorial caribbean damselfishes. Ecology 77, 885–899.CrossRefGoogle Scholar
Sahni, SK and Rydkina, E (2009) Host-cell interactions with pathogenic Rickettsia species. Future Microbiology 4, 323–339.CrossRefGoogle ScholarPubMed
Scott, ME and Dobson, A (1989) The role of parasites in regulating host abundance. Parasitology Today 5, 176–183.CrossRefGoogle ScholarPubMed
Short, S, Guler, Y, Yang, G, Kille, P and Ford, AT (2012) Paramyxean-microsporidian co-infection in amphipods: is the consensus that Microsporidia can feminise their hosts presumptive? International Journal for Parasitology 42, 683–691.CrossRefGoogle ScholarPubMed
Sibley, LD (2004) Intracellular parasite invasion strategies. Science (New York, N.Y.) 304, 248–253.CrossRefGoogle ScholarPubMed
Tamim El Jarkass, H and Reinke, AW (2020) The ins and outs of host-microsporidia interactions during invasion, proliferation and exit. Cellular Microbiology 22, e13247.CrossRefGoogle ScholarPubMed
Terry, RS, Smith, JE, Sharpe, RG, Rigaud, T, Timothy, D, Littlewood, J, Ironside, JE, Rollinson, D, Bouchon, D, Macneil, C, Dick, JTA and Dunn, AM (2004) Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society B: Biological Sciences 271, 1783–1789.CrossRefGoogle ScholarPubMed
Tham, AC and Sanjay, S (2012) Clinical spectrum of microsporidial keratoconjunctivitis. Clinical and Experimental Ophthalmology 40, 512–518.CrossRefGoogle ScholarPubMed
Thomas, F and Poulin, R (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431–436.CrossRefGoogle ScholarPubMed
Walker, DH (1995) Rocky Mountain spotted fever: a seasonal alert. Clinical Infectious Diseases 20, 1111–1117.CrossRefGoogle ScholarPubMed
Weinert, LA, Werren, JH, Aebi, A, Stone, GN and Jiggins, FM (2009) Evolution and diversity of Rickettsia bacteria. BMC Biology 7, 1–15.CrossRefGoogle ScholarPubMed
White, TA, Campbell, BD, Kemp, PD and Hunt, CL (2000) Sensitivity of three grassland communities to simulated extreme temperature and rainfall events. Global Change Biology 6, 671–684.CrossRefGoogle Scholar
Wickham, H (2011) ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics 3, 180–185.CrossRefGoogle Scholar
Wolinska, J, Seda, J, Koerner, H, Smilauer, P and Petrusek, A (2011) Spatial variation of Daphnia parasite load within individual water bodies. Journal of Plankton Research 33, 1284–1294.CrossRefGoogle Scholar
Woodin, SA (1974) Polychaete abundance patterns in a marine soft-sediment environment: the importance of biological interactions. Ecological Monographs 44, 171–187.CrossRefGoogle Scholar
Zhu, X, Wittner, M, Tanowitz, HB, Kotler, D, Cali, A and Weiss, LM (1993) Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. Journal of infectious Diseases 168, 1570–1575.CrossRefGoogle ScholarPubMed