The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection

Berger, Chloé Suzanne; Aubin‐Horth, Nadia

doi:10.1098/rspb.2020.0412

Cited by 12 publications

(14 citation statements)

References 46 publications

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“…These discoveries might also allow scientist to question and build novel hypotheses on the underlying mechanisms that drive S . solidus infection success, mate choice, population structure, reproductive isolation, or behavioural manipulation (Berger & Aubin‐Horth, 2020; Henrich & Kalbe, 2016; Jager & Schjorring, 2006; Schjørring, 2009; Sprehn et al, 2015). Herein, we also demonstrate that the host microbiome, which varies with host genotype in healthy individuals, is impacted by exposure to parasites and depends on the parasite genotype in infected individuals.…”

Section: Discussionmentioning

confidence: 99%

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

et al. 2022

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A growing literature demonstrates the impact of helminths on their host gut microbiome. We investigated whether the stickleback host microbiome depends on ecoevolutionary variables by testing the impact of exposure to the cestode parasite Schistocephalus solidus with respect to infection success, host genotype, parasite genotype, and parasite microbiome composition. We observed constitutive differences in the microbiome of sticklebacks of different origin, and those differences increased when sticklebacks exposed to the parasite resisted infection. In contrast, the microbiome of successfully infected sticklebacks varied with parasite genotype. More specifically, we revealed that the association between microbiome and immune gene expression increased in infected individuals and varied with parasite genotype. In addition, we showed that S. solidus hosts a complex endomicrobiome and that bacterial abundance in the parasite correlates with expression of host immune genes. Within this comprehensive analysis we demonstrated that (i) parasites contribute to modulating the host microbiome through both successful and unsuccessful infection, (ii) when infection is successful, the host microbiome varies with parasite genotype due to genotype‐dependent variation in parasite immunomodulation, and (iii) the parasite‐associated microbiome is distinct from its host and impacts the host immune response to infection.

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Section: Discussionmentioning

confidence: 99%

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

et al. 2022

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“…Threespine stickleback is a model for behavioural biology (Huntingford and Ruiz-Gomez, 2009) but also for the study of host-parasite relationships (Barber and Scharsack, 2010). Schistocephalus solidus infection influence threespine sticklebacks behaviour and physiology (Berger et al, 2021; Berger and Aubin-Horth, 2020; Grécias et al, 2018, 2017; Hébert et al, 2017; Øverli et al, 2001; Quinn et al, 2012; Scharsack et al, 2007; Talarico et al, 2017). In particular, serotoninergic turnover is decreased in the brain of infected fish (Øverli et al, 2001) and serotoninergic activity is involved in the control of locomotor activity (Winberg et al, 1993).…”

Section: Discussionmentioning

confidence: 99%

“…The day before the experiment, individuals were isolated in 2L water tanks without food. On the first day of the experiment (in the morning, see Figure 1), the behaviour of each fish was measured in a 45L test aquarium with white plexiglass-covered walls using standard behaviour test to measure exploration and predator response in threespine stickleback (Berger and Aubin-Horth, 2020;Grécias et al, 2018Grécias et al, , 2017. All fishes were re-fed at the end of the behaviour test and then fed twice a day as before.…”

Section: Experimental Design and Samplingmentioning

confidence: 99%

Association between the magnitude of melatonin circadian rhythm and personality in the threespine stickleback

Philippe¹,

Aubin‐Horth²

2023

Preprint

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Melatonin secretion follows a circadian pattern with a maximum level at night in many species. However, in zebrafish (Danio rerio, a diurnal fish species) large inter-individual variations in daily rhythmicity of melatonin levels are present and are associated with variation in behaviour. Melatonin secretion rhythm of proactive individuals that are more active and exploratory are of larger amplitude compared to reactive individuals. In threespine sticklebacks (Gasterosteus aculeatus), a nocturnal species, inter-individual variability of behaviour is well described. However, inter-individual variation of melatonin rhythm and its association with variation in behaviour has never been measured in this species, which would allow to test if patterns found in zebrafish can be generalized for diurnal and nocturnal species. We measured large inter-individual variation in melatonin levels and found that activity was positively correlated with plasma melatonin concentration measured at night. We did not observe any significant difference in nigh-day variation in melatonin concentration between very active and less active groups. However, we found that individuals classified as reactive based on their propensity to wall-hugging, a measure of anxiety in fish, showed large variation in melatonin between night and day, while this rhythm was not seen in proactive individuals that frequently used the center of the aquarium.Overall, our study suggests that melatonin may directly modulate behaviour in wild sticklebacks, and that while interindividual variation in melatonin rhythm may be widespread in fish, but with different pattern of variation depending on the species.

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“…However, it is clear that further empirical and theoretical work is needed that properly considers both active, i.e. the secretion of parasite chemical messengers that directly affect host brain function 54 , and passive, mechanisms to unravel the relative roles they may play in driving host behaviour.…”

Section: Discussionmentioning

confidence: 99%

Schistocephalus parasite infection alters sticklebacks’ movement ability and thereby shapes social interactions

Jolles

Mazué

Davidson

et al. 2020

Sci Rep

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Parasitism is ubiquitous in the animal kingdom. Although many fundamental aspects of host-parasite relationships have been unravelled, few studies have systematically investigated how parasites affect organismal movement. Here we combine behavioural experiments of Schistocephalus solidus infected sticklebacks with individual-based simulations to understand how parasitism affects individual movement ability and thereby shapes social interaction patterns. High-resolution tracking revealed that infected fish swam, accelerated, and turned more slowly than did non-infected fish, and tended to be more predictable in their movements. Importantly, the strength of these effects increased with increasing parasite load (proportion of body weight), with more heavily infected fish showing larger changes and impairments in behaviour. When grouped, pairs of infected fish moved more slowly, were less cohesive, less aligned, and less temporally coordinated than non-infected pairs, and mixed pairs were primarily led by the non-infected fish. These social patterns also emerged in simulations of self-organised groups composed of individuals differing similarly in speed and turning tendency, suggesting infection-induced changes in mobility and manoeuvrability may drive collective outcomes. Together, our results demonstrate how infection with a complex life-cycle parasite affects the movement ability of individuals and how this in turn shapes social interaction patterns, providing important mechanistic insights into the effects of parasites on host movement dynamics. Parasitism is ubiquitous across the animal kingdom, with parasites often exerting considerable influence on their hosts by consuming energy and inducing morphological, physiological, and behavioural changes 1-3. Parasites have been best studied in terms of their ecological and evolutionary effects on hosts 1,4 , but may also have large effects on host behaviour 2. Besides potential manipulation of the host, parasites also often change their host's morphology and physiology, which may strongly alter its movement dynamics 2,5 , such as by reducing the energy available to allocate to movement or by compromising their movement capacity and mobility. So far, few studies have systematically investigated the mechanistic basis of such potential behavioural modifications 2,5 or considered the repercussions this may have for social interactions and collective outcomes via self-organising effects 6,7. Three-spined sticklebacks (Gasterosteus aculeatus) infected with the flatworm Schistocephalus solidus are a host-parasite model system with well-documented parasite effects on host behaviour 8,9. S. solidus is a complex life-cycle parasite that has to sequentially infect a copepod, the three-spined stickleback, and a fish-eating bird to survive and reproduce. It is often proposed that parasites with complex life cycles manipulate their host's behaviour in order to increase their probability of transmission to their final host 4. However, the parasite may also affect behaviour via energ...

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The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection

Cited by 12 publications

References 46 publications

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

Association between the magnitude of melatonin circadian rhythm and personality in the threespine stickleback

Schistocephalus parasite infection alters sticklebacks’ movement ability and thereby shapes social interactions

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