Parasites are just the strings: Microbes as the real puppet masters in phenotypic manipulations of parasitized animals

This blog post is provided by Priscila Salloum, Fátima Jorge and Robert Poulin and tells the #StoryBehindThePaper for the paper “Inter-individual variation in parasite manipulation of host phenotype: a role for parasite microbiomes?“, which was recently published in the Journal of Animal Ecology. They explore how differences in the microbiome of parasites might impact the way that those parasites can manipulate their hosts’ behaviour.

Many parasites have the impressive ability of bending their hosts’ will, manipulating the host’s phenotype or behaviour, like real puppet masters. You have probably heard about the hairworm that makes its cricket host jump into water so that the mature worm can come out in its perfect environment – water. Or you might have seen something about parasitised animals that become less conspicuous and are more easily found by their predators, the parasite’s definitive host (Figure 1). However, there is great variability in host behavioural manipulation induced by parasites, and a real gradation in possible levels of manipulation achieved in individual parasite-host interactions.

Figure 1.  The parasite Profilicollis novaezealandiae infecting a shore crab in New Zealand, for which infection levels seem correlated with changes in hiding behaviour1. (Photo credit: Jerusha Bennett)

When the mechanisms underlying phenotypic manipulation are known, they involve alterations in the hosts’ neural system, hormones, or immune response, or even a direct change in the expression of genes responsible for specific host behaviours. These alterations happen to a different degree in different individuals. If the host’s phenotypic manipulation induced by the parasite had a fixed outcome, we would expect to see most infected hosts with a similar manipulated phenotype. Intuitively, we could be thinking that there is an evolutionary benefit for the parasite in manipulating the phenotype of its host, and that an ‘optimal’ phenotype would be the ideal outcome for the parasite. However, there is not enough evidence in support of such narrow outcomes from phenotypic manipulation in parasitised animals, and in fact, the phenotypic variability after parasitic infection is as broad as in uninfected animals (Figure 2). So, what causes this great variability? To a certain extent, genetic and non-genetic factors such as age or body condition of both the host and the parasite, as well as environmental differences. But much of the variation remains unexplained.

Figure 2. The relationship between infected and uninfected hosts shows highly variable phenotypes also after infection, supporting that there is not a narrow outcome of phenotypic manipulation by parasites, whether the parasite is transmitted by predation of the intermediate host (yes, blue) or not (no, red). (Figure credit: Priscila Salloum, based on data from Nakagawa et al.2)

In an invited perspective piece in the Journal of Animal Ecology, we considered a different take on the reasons for the variation in parasite-induced phenotypic manipulations, proposing a hypothesis and potential research directions for the future. With the growing knowledge of the importance of microbiomes in shaping so many aspects of all organisms on Earth, our hypothesis is that differences in the composition and abundance of specific microbes associated with the parasites may play a large role in the outcome of parasite-induced host manipulation. Embracing the holobiome concept, microbes inhabiting the parasite have their own set of genes which will contribute towards the evolution of parasite and microbes as a whole and unique entity, fine-tuned to getting the best out of their environment (be it microbes getting the best out of their parasites, or both getting the best out of the parasitised host). This means that instead of looking at parasite-host interactions as a two-dimensional system, we should be looking at multi-dimensional interactions happening within the parasite (with its microbiome), between the parasite’s microbiome and the animal host’s microbiome, and between the parasite and the animal host (which also extends to the interactions of the animal host with its own microbiome, but this is not the matter we focus on).

Suppose that, apart from the parasites’ microbiome, all else is similar among parasites and among their hosts (i.e. genes, environment, etc). In this case, the presence or abundance of certain microbes within a parasite would determine the magnitude of the changes induced in the host. The microbes, in symbiosis with the parasite, will benefit from parasitic transmission to their next animal host: if the parasite (which is their ‘home and resource’) is successful, the microbes will also prevail. Thus, the outcome of phenotypic manipulation matters as much to the evolution of the parasite as it matters to the evolution of its microbiome. There are two underlying assumptions to such a statement:

  1. The microbiome of the parasite is different from the microbiome of its hosts, which has been demonstrated before, supporting our hypothesis3,4;
  2. Microbes are transmitted among life-stages (or different generations) of the parasite, which has also been demonstrated before5, so also supports our hypothesis.

The microbiome of different individual parasites has a different composition and abundance of microbes, with great variation even among individual parasites of the same population. This is caused by processes like acquiring microbes from different sources from the previous generation (such as with diet), competition among lineages within a parasite, and because not all microbes from the parent parasite will succeed in being transferred to its offspring. Such variation in the microbiome of individual parasites may be linked to variability in the levels of parasite-induced host phenotypic manipulation (Figure 3). That is, parasites with different microbiomes may have different impacts on the phenotype of their hosts.

Figure 3. Schematic representation of possible changes in the phenotype (colour) of an amphipod host induced by an acanthocephalan parasite (represented by a black outline within the amphipod shades), correlated with microbiome composition and abundance (represented by the small shapes inside the acanthocephalan). (Figure credit: Poulin et al., 20226).

There are examples of individual microbes interacting with parasites in manipulating the phenotype of their hosts7-10. Now consider that many different microbes in the parasite`s microbiome contribute to changes in the phenotype of the parasitised host. Going forward, microbiome characterisations of both parasites and their hosts using -omics approaches can lead to finding relevant molecules in the mechanics of phenotypic change, assigning molecules to specific genes (and their organism), and potentially silencing these genes to assess their importance in inducing phenotypic change. Additionally, modifying the microbiome of parasites with antibiotics treatment, and assessing the phenotypic change of organisms infected with control and treated parasites can lead to more direct evidence of the importance of the many-fold microbial players in parasite-induced host phenotypic manipulation. Should we be calling it holobiome-induced host phenotypic manipulation?

About the authors

Robert Poulin has been at the University of Otago for 30 years, during which his research has explored host-parasite interactions from multiple ecological and evolutionary perspectives, across all taxa and using a broad range of approaches.

Fátima Jorge was a postdoctoral fellow at the University of Otago where she applied a wide range of multidisciplinary approaches to investigate the (co)evolutionary patterns of parasite diversification, and the role and diversity of the microbiota within and across host-parasite-microbe interactions.

Priscila Salloum is a postdoctoral fellow at the University of Otago. She is interested in understanding mechanisms driving phenotypic diversification and adaptation, and is applying her genomics background to uncover the roles of the microbiota in the phenotypic changes linked to parasitic infections.

Find out more about the Evolutionary and Ecological Parasitology Research Group here.

Read the paper

Read the full paper here: Poulin, R., Jorge, F., & Salloum, P. M. (2022). Inter-individual variation in parasite manipulation of host phenotype: A role for parasite microbiomes?. Journal of Animal Ecology, 00, 1– 6. https://doi.org/10.1111/1365-2656.13764

References
  1. Latham, A., & Poulin, R. (2002). Effect of acanthocephalan parasites on hiding behaviour in two species of shore crabs. Journal of Helminthology, 76(4), 323-326. doi:10.1079/JOH2002139
  2. Nakagawa, S., Poulin, R., Mengersen, K., Reinhold, K., Engqvist, L., Lagisz, M., & Senior, A. M. (2015). Meta-analysis of variation: ecological and evolutionary applications and beyond. Methods in Ecology and Evolution, 6, 143–152.
  3. Jorge, F., Dheilly, N. M., & Poulin, R. (2020). Persistence of a core microbiome through the ontogeny of a multi-host parasite. Frontiers in Microbiology, 11, 954. https://doi.org/10.3389/fmicb.2020.00954
  4. Jorge, F., Dheilly, N. M., Froissard, C., Wainwright, E., & Poulin, R. (2022a). Consistency of bacterial communities in a parasitic worm: variation throughout the life cycle and across geographic space. Microbial Ecology, 83, 724–738.
  5. Vaughan, J. A., Tkach, V. V., & Greiman, S. E. (2012). Neorickettsial endosymbionts of the Digenea: diversity, transmission and distribution. Advances in Parasitology, 79, 253–297.
  6. Poulin, R., Jorge, F., Salloum, P. (2022). Inter-individual variation in parasite manipulation of host phenotype: a role for parasite microbiomes? Journal of Animal Ecology, 00, 1-6. doi: 10.1111/1365-2656.13764
  7. Kaiser, W., Huguet, E., Casas, J., Commin, C., & Giron, D. (2010). Plant green-island phenotype induced by leaf-miner is mediated by bacterial symbionts. Proceedings of the Royal Society B, 277, 2311–2319.
  8. Frago, E., Dicke, M., & Godfray, H. C. J. (2012). Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology and Evolution, 27, 705–711.
  9. Goodrich-Blair, H., & Clarke, D. J. (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Molecular Microbiology, 64, 260–268.
  10. Dheilly, N. M., Maure, F., Ravallec, M., Galinier, R., Doyon, J., Duval, D., Leger, L., Volkoff, A.-N., Missé, D., Nidelet, S., Demolombe, V., Brodeur, J., Gourbal, B., Thomas, F., & Mitta, G. (2015b). Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proceedings of the Royal Society B, 282, 20142773.

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