Anxiety and parasitism in an aquatic invertebrate: evolutive and mechanistic approaches

Defended on the 28th August 2020

Funding: French ministry of research

Supervisor: Marie-Jeanne Perrot-Minnot ; cosupervisor: Frank Cézilly

Started in October 2017

Abstract

Trophically transmitted parasites induce changes in their host’s phenotype. These changes are supposed to increase transmission probability to definitive hosts through the predation of intermediate hosts. This phenomenon is known as ‘parasite manipulation’ has been hypothesized to be an adaptive trait of parasites for a long time. As manipulation involves predator-prey interactions, it is therefore necessary to understand how antipredatory behaviours are modulated by exogenous (predation pressure) and endogenous (infection, emotional state) factors. We tried to go into this phenomenon in depth, in amphipods, by responding to several questions : (1) what is the extent of the multidimensionality in parasite manipulation by Acanthocephalan, quantified through a meta-analysis ; (2) is there variation in the magnitude of antipredatory behaviours according to local predation risk? (3) are antipredatory behaviours flexible with respect to local predation risk? (4) Do parasites exploit behavioural flexibility in uninfected individuals, in relation to an emotional state such as anxiety-like state? Within the Acanthocephala phylum, we evidenced notable changes, more particularly of host antipredatory behaviours (microhabitat changes, protection and responses to stimuli). Considering Gammarus fossarum, Pomphorhynchus tereticollis host-parasite couple, we showed that there was variation in the magnitude of antipredatory behavioural changes induced by infection (phototaxy and refuge use), with respect to local predation risk : host manipulation seemed as strong as predation risk, i.e. transmission opportunities, is low. With a correlational approach, we also evidenced variation in the magnitude of antipredatory behaviours according to local predation risk and conspecifics density, in uninfected individuals. In addition, we emphasized flexibility of behavioural responses to predator cues: individuals from populations experiencing high predation risk exhibited increased responses as predator cues concentrations increased. In contrast, individuals from populations experiencing low predation risk appeared to exhibit strong responses independent of predator cues concentrations, suggesting hypersensitivity. We supposed that these strategies would be closely related to the exposure to chronic predation risk. We therefore suggest the existence of an anxiety-like state that could result from the repetition of acute stress, i.e. fear, episodes. We made a first step through an experimental approach, evidencing the existence of both anxiety-like and fear behaviours in G. fossarum. Overall, these works pointed out the importance of predator-prey interactions in the study of parasite manipulation. More particularly, we evidenced variation and complex modulation of host antipredatory behaviours in accordance with local predation risk, and which may be closely related to an emotional state stemming from chronic predation stress. We therefore suggest some future directions to investigate, such as the underlying mechanisms of anxiety-like state, and the role of parasite in the modulation of this state that would modify the expression of antipredatory behaviours.

Keywords

Gammarus fossarum, acanthocephala, amphipoda, behaviour, emotional state, parasite manipulation, predation

Jury

Jean-Nicolas Beisel, ENGEES, université de Strasbourg – reviewer
Anne-Sophie Darmaillacq, université de Caen – reviewer
Jean-François Ferveur, université Bourgogne Franche-Comté – examiner
Vincent Médoc, université de Saint-Etienne – examiner
Marie-Jeanne Perrot-Minnot, université Bourgogne Franche-Comté – supervisor
Thierry Rigaud, université Bourgogne Franche-Comté – examiner

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Anxiety and parasitism in an aquatic invertebrate: evolutive and mechanistic approaches

Defended on the 28th August 2020

Funding: French ministry of research

Supervisor: Marie-Jeanne Perrot-Minnot ; cosupervisor: Frank Cézilly

Started in October 2017

 

Abstract

Trophically transmitted parasites induce changes in their host’s phenotype. These changes are supposed to increase transmission probability to definitive hosts through the predation of intermediate hosts. This phenomenon is known as ‘parasite manipulation’ has been hypothesized to be an adaptive trait of parasites for a long time. As manipulation involves predator-prey interactions, it is therefore necessary to understand how antipredatory behaviours are modulated by exogenous (predation pressure) and endogenous (infection, emotional state) factors. We tried to go into this phenomenon in depth, in amphipods, by responding to several questions : (1) what is the extent of the multidimensionality in parasite manipulation by Acanthocephalan, quantified through a meta-analysis ; (2) is there variation in the magnitude of antipredatory behaviours according to local predation risk? (3) are antipredatory behaviours flexible with respect to local predation risk? (4) Do parasites exploit behavioural flexibility in uninfected individuals, in relation to an emotional state such as anxiety-like state? Within the Acanthocephala phylum, we evidenced notable changes, more particularly of host antipredatory behaviours (microhabitat changes, protection and responses to stimuli). Considering Gammarus fossarum, Pomphorhynchus tereticollis host-parasite couple, we showed that there was variation in the magnitude of antipredatory behavioural changes induced by infection (phototaxy and refuge use), with respect to local predation risk : host manipulation seemed as strong as predation risk, i.e. transmission opportunities, is low. With a correlational approach, we also evidenced variation in the magnitude of antipredatory behaviours according to local predation risk and conspecifics density, in uninfected individuals. In addition, we emphasized flexibility of behavioural responses to predator cues: individuals from populations experiencing high predation risk exhibited increased responses as predator cues concentrations increased. In contrast, individuals from populations experiencing low predation risk appeared to exhibit strong responses independent of predator cues concentrations, suggesting hypersensitivity. We supposed that these strategies would be closely related to the exposure to chronic predation risk. We therefore suggest the existence of an anxiety-like state that could result from the repetition of acute stress, i.e. fear, episodes. We made a first step through an experimental approach, evidencing the existence of both anxiety-like and fear behaviours in G. fossarum. Overall, these works pointed out the importance of predator-prey interactions in the study of parasite manipulation. More particularly, we evidenced variation and complex modulation of host antipredatory behaviours in accordance with local predation risk, and which may be closely related to an emotional state stemming from chronic predation stress. We therefore suggest some future directions to investigate, such as the underlying mechanisms of anxiety-like state, and the role of parasite in the modulation of this state that would modify the expression of antipredatory behaviours.

Keywords

Gammarus fossarum, acanthocephala, amphipoda, behaviour, emotional state, parasite manipulation, predation

 

Jury

Jean-Nicolas Beisel, ENGEES, université de Strasbourg – reviewer
Anne-Sophie Darmaillacq, université de Caen – reviewer
Jean-François Ferveur, université Bourgogne Franche-Comté – examiner
Vincent Médoc, université de Saint-Etienne – examiner
Marie-Jeanne Perrot-Minnot, université Bourgogne Franche-Comté – supervisor
Thierry Rigaud, université Bourgogne Franche-Comté – examiner