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

2019 ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Nadia Aubin-Horth
Keyword(s):  
Gasterosteus Aculeatus ◽  
Final Host ◽  
Life Cycles ◽  
Avian Host ◽  
Allopatric Population ◽  
Late Infection ◽  
Intermediate Hosts ◽  
Behavioural Changes ◽  
Schistocephalus Solidus ◽  
Host Parasite

ABSTRACTParasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of Schistocephalus solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial, and that local adaptation between host-parasite pairs may extend to the response to the parasite’s secretome content.

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

2020 ◽  
Vol 287 (1925) ◽  
pp. 20200412 ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Nadia Aubin-Horth
Keyword(s):  
Gasterosteus Aculeatus ◽  
Final Host ◽  
Life Cycles ◽  
Avian Host ◽  
Allopatric Population ◽  
Late Infection ◽  
Intermediate Hosts ◽  
Behavioural Changes ◽  
Host Parasite ◽  
Host Behaviour

Parasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus , and its intermediate host, the threespine stickleback ( Gasterosteus aculeatus ), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host–parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host–parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of S. solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial and that local adaptation between host–parasite pairs may extend to the response to the parasite's secretome content.

scholarly journals Host behavior alteration by its parasite: from brain gene expression to functional test

2020 ◽  
Author(s):  
Lucie Grecias ◽  
Francois Olivier Hebert ◽  
Verônica Angelica Alves ◽  
Iain Barber ◽  
Nadia Aubin-Horth
Keyword(s):  
Gene Expression ◽  
Gasterosteus Aculeatus ◽  
Expression Profiles ◽  
Infected Fish ◽  
Life Cycles ◽  
Avian Host ◽  
Intermediate Hosts ◽  
Altered Expression ◽  
Brain Gene Expression ◽  
Successful Infection

ABSTRACTMany parasites with complex life cycles modify their intermediate hosts’ behaviour, presumably to increase transmission to their final host. The threespine stickleback (Gasterosteus aculeatus) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S.solidus to determine the proximal causes of these behavioural alterations. We show that infected fish have altered expression levels in genes involved in the inositol pathway. We thus tested the functional implication of this pathway and successfully rescued normal behaviours in infected sticklebacks using lithium exposure. We also show that exposed but uninfected fish have a distinct gene expression profile from both infected fish and control individuals, allowing us to separate gene activity related to parasite exposure from consequences of a successful infection. Finally, we find that Selective Serotonin Reuptake Inhibitor (SSRI)-treated sticklebacks and infected fish do not have similarly altered gene expression, despite their comparable behaviours, suggesting that the serotonin pathway is probably not the main driver of phenotypic changes in infected sticklebacks. Taken together, our results allow us to predict that if S.solidus directly manipulates its host, it could target the inositol pathway.

scholarly journals Major host transitions are modulated through transcriptome-wide reprograming events in Schistocephalus solidus, a threespine stickleback parasite

2016 ◽  
Author(s):  
François Olivier Hébert ◽  
Stephan Grambauer ◽  
Iain Barber ◽  
Christian R Landry ◽  
Nadia Aubin-Horth
Keyword(s):  
Life Cycle ◽  
Intermediate Host ◽  
Final Host ◽  
Life Cycles ◽  
Threespine Stickleback ◽  
Complex Life Cycle ◽  
Ecological Niches ◽  
Avian Host ◽  
Complex Life Cycles ◽  
Schistocephalus Solidus

ABSTRACTParasites with complex life cycles have developed numerous phenotypic strategies, closely associated with developmental events, to enable the exploitation of different ecological niches and facilitate transmission between hosts. How these environmental shifts are regulated from a metabolic and physiological standpoint, however, still remain to be fully elucidated. We examined the transcriptomic response of Schistocephalus solidus, a trophically-transmitted parasite with a complex life cycle, over the course of its development in an intermediate host, the threespine stickleback, and the final avian host. Results from our differential gene expression analysis show major reprogramming events among developmental stages. The final host stage is characterized by a strong activation of reproductive pathways and redox homeostasis. The attainment of infectivity in the fish intermediate host – which precedes sexual maturation in the final host and is associated with host behaviour changes – is marked by transcription of genes involved in neural pathways and sensory perception. Our results suggest that un-annotated and S. solidus-specific genes could play a determinant role in host-parasite molecular interactions required to complete the parasite’s life cycle. Our results permit future comparative analyses to help disentangle species-specific patterns of infection from conserved mechanisms, ultimately leading to a better understanding of the molecular control and evolution of complex life cycles.

scholarly journals Host behaviour alteration by its parasite: from brain gene expression to functional test

2020 ◽  
Vol 287 (1938) ◽  
pp. 20202252
Author(s):  
Lucie Grecias ◽  
Francois Olivier Hebert ◽  
Verônica Angelica Alves ◽  
Iain Barber ◽  
Nadia Aubin-Horth
Keyword(s):  
Gene Expression ◽  
Gasterosteus Aculeatus ◽  
Expression Profiles ◽  
Infected Fish ◽  
Life Cycles ◽  
Avian Host ◽  
Intermediate Hosts ◽  
Altered Expression ◽  
Brain Gene Expression ◽  
Successful Infection

Many parasites with complex life cycles modify their intermediate hosts' behaviour, presumably to increase transmission to their final host. The threespine stickleback ( Gasterosteus aculeatus ) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S. solidus to determine the proximal causes of these behavioural alterations. We show that infected fish have altered expression levels in genes involved in the inositol pathway. We thus tested the functional implication of this pathway and successfully rescued normal behaviours in infected sticklebacks using lithium exposure. We also show that exposed but uninfected fish have a distinct gene expression profile from both infected fish and control individuals, allowing us to separate gene activity related to parasite exposure from consequences of a successful infection. Finally, we find that selective serotonin reuptake inhibitor-treated sticklebacks and infected fish do not have similarly altered gene expression, despite their comparable behaviours, suggesting that the serotonin pathway is probably not the main driver of phenotypic changes in infected sticklebacks. Taken together, our results allow us to predict that if S. solidus directly manipulates its host, it could target the inositol pathway.

scholarly journals The three-spined stickleback-Schistocephalus solidussystem: an experimental model for investigating host-parasite interactions in fish

Parasitology ◽  
2009 ◽  
Vol 137 (3) ◽  
pp. 411-424 ◽  
Author(s):  
I. BARBER ◽  
J. P. SCHARSACK
Keyword(s):  
Immune Responses ◽  
Gasterosteus Aculeatus ◽  
Laboratory Model ◽  
Host Fish ◽  
Schistocephalus Solidus ◽  
Host Parasite Interactions ◽  
Experimental Laboratory ◽  
Host Parasite ◽  
Host Behaviour

SUMMARYPlerocercoids of the pseudophyllidean cestodeSchistocephalus solidusinfect the three-spined sticklebackGasterosteus aculeatus, with important consequences for the biology of host fish. Techniques for culturing the parasitein vitroand generating infective stages that can be used to infect sticklebacks experimentally have been developed, and the system is increasingly used as a laboratory model for investigating aspects of host-parasite interactions. Recent experimental laboratory studies have focused on the immune responses of hosts to infection, the consequences of infection for the growth and reproductive development of host fish and the effects of infection on host behaviour. Here we introduce the host and the parasite, review the major findings of these recent experimental infection studies and identify further aspects of host parasite interactions that might be investigated using the system.

scholarly journals The helminth infracommunities of the wood mouse (Apodemus sylvaticus) two years after the fire in Mediterranean forests

2013 ◽  
Vol 50 (1) ◽  
pp. 27-38 ◽  
Author(s):  
I. Torre ◽  
A. Arrizabalaga ◽  
C. Feliu ◽  
A. Ribas
Keyword(s):  
Species Richness ◽  
Life Cycle ◽  
Wood Mouse ◽  
Final Host ◽  
Life Cycles ◽  
Helminth Species ◽  
Mediterranean Forests ◽  
Intermediate Hosts ◽  
Wood Mice ◽  
Short Period

AbstractParasites have been recognized as indicators for natural or man-induced environmental stress and perturbation. In this article, we investigated the role of two non-exclusive hypotheses on the response of helminths of wood mice to fire perturbation: 1) a reduction of the helminth infracommunity (species richness) in post-fire areas due to the temporal lack of worms with indirect (complex) life cycles linked to intermediate hosts that are more specialized than the final host, and 2) an increase of the abundance of helminths with direct (simple) life cycles as a response of increasing abundances of the final host, may be in stressful conditions linked to the post-fire recolonization process.We studied the helminth infracommunities of 97 wood mice in two recently burned plots (two years after the fire) and two control plots in Mediterranean forests of NE Spain. Species richness of helminths found in control plots (n = 14) was twice large than in burned ones (n = 7). Six helminth species were negatively affected by fire perturbation and were mainly or only found in unburned plots. Fire increased the homogeneity of helminth infracommunities, and burned plots were characterised by higher dominance, and higher parasitation intensity. We found a gradient of frequency of occurrence of helminth species according to life cycle complexity in burned areas, being more frequent monoxenous (66.6 %), than diheteroxenous (33.3 %) and triheteroxenous (0 %), confirming the utility of helminths as bioindicators for ecosystem perturbations. Despite the short period studied, our results pointed out an increase in the abundance and prevalence of some direct life cycle helminths in early postfire stages, whereas indirect life cycle helminths were almost absent. A mismatch between the final host (that showed a fast recovery shortly after the fire), and the intermediate hosts (that showed slow recoveries shortly after the fire), was responsible for the loss of half of the helminth species.

Estimating effective population size for a cestode parasite infecting three-spined sticklebacks

Parasitology ◽  
2019 ◽  
Vol 146 (07) ◽  
pp. 883-896
Author(s):  
Hannah M. Strobel ◽  
Sara J. Hays ◽  
Kristine N. Moody ◽  
Michael J. Blum ◽  
David C. Heins
Keyword(s):  
Population Size ◽  
Effective Population Size ◽  
Gasterosteus Aculeatus ◽  
Microsatellite Data ◽  
Effective Population ◽  
Cestode Parasite ◽  
Schistocephalus Solidus ◽  
Host Parasite Interactions ◽  
Parasite Evolution ◽  
Host Parasite

AbstractRemarkably few attempts have been made to estimate contemporary effective population size (Ne) for parasitic species, despite the valuable perspectives it can offer on the tempo and pace of parasite evolution as well as coevolutionary dynamics of host–parasite interactions. In this study, we utilized multi-locus microsatellite data to derive single-sample and temporal estimates of contemporaryNefor a cestode parasite (Schistocephalus solidus) as well as three-spined stickleback hosts (Gasterosteus aculeatus) in lakes across Alaska. Consistent with prior studies, both approaches recovered small and highly variable estimates of parasite and hostNe. We also found that estimates of hostNeand parasiteNewere sensitive to assumptions about population genetic structure and connectivity. And, while prior work on the stickleback–cestode system indicates that physiographic factors external to stickleback hosts largely govern genetic variation inS. solidus, our findings indicate that stickleback host attributes and factors internal to the host – namely body length, genetic diversity and infection – shape contemporaryNeof cestode parasites.

Incidence and intensity of Cyathocephalus truncatus and Schistocephalus solidus infection in Gasterosteus aculeatus

1982 ◽  
Vol 60 (5) ◽  
pp. 1091-1095 ◽  
Author(s):  
T. E. Reimchen
Keyword(s):  
Gasterosteus Aculeatus ◽  
Attachment Site ◽  
Relative Increase ◽  
Infected Fish ◽  
Host Feeding ◽  
Infection Rates ◽  
Intermediate Hosts ◽  
Queen Charlotte Islands ◽  
Schistocephalus Solidus ◽  
Different Seasons

Cyathocephalus truncatus, a cestode usually found in salmonids, and plerocercoids of Schistocephalus solidus are reported from a population of Gasterosteus aculeatus on the Queen Charlotte Islands, British Columbia. Adult C. truncatus attached at the anterior of the intestine adjacent to the pyloric sphincter, whereas in salmonids the pyloric caeca is the usual attachment site. Mean intensities of infection for C. truncatus and S. solidus were 2.7 (maximum 26) and 3.4 (maximum 87), respectively, with intensities increasing in larger fish. The highest incidence of C. truncatus infection was from February to May (80%) and for S. solidus, from April to September (50%). Infection rates for C. truncatus during different seasons and among different length classes offish were directly correlated with the relative abundance of amphipods (the intermediate hosts of C. truncatus) in the fish stomachs. Possible modification of host feeding behaviour is indicated by a relative increase in the consumption of amphipods by infected fish.

scholarly journals Stage-dependent behavioural changes but early castration induced by the acanthocephalan parasite Polymorphus minutus in its Gammarus pulex intermediate host

Parasitology ◽  
2017 ◽  
Vol 145 (3) ◽  
pp. 260-268 ◽  
Author(s):  
YANN BAILLY ◽  
FRANK CÉZILLY ◽  
THIERRY RIGAUD
Keyword(s):  
Significant Variation ◽  
Developmental Stages ◽  
Life Cycles ◽  
Gammarus Pulex ◽  
Complex Life Cycles ◽  
Behavioural Changes ◽  
Single Mechanism ◽  
Behavioural Alteration ◽  
Host Parasite ◽  
Acanthocephalan Parasite

SUMMARYMultidimensionality in parasite-induced phenotypic alterations (PIPA) has been observed in a large number of host–parasite associations, particularly in parasites with complex life cycles. However, it is still unclear whether such a syndrome is due to the successive activation of independent PIPAs, or results from the synchronous disruption of a single mechanism. The aim of the present study was to investigate the onset and progression of two PIPAs (a behavioural alteration: reversion of geotaxis, and castration) occurring in the crustacean amphipod Gammarus pulex infected with the acanthocephalan Polymorphus minutus, at different parasite developmental stages. Modifications of geotaxis in hosts differed according to the parasite developmental stage. Whereas the cystacanth stage induced a negative geotaxis (exposing the gammarid to predation by birds, the definitive hosts), the acanthella stage, not yet infective for the definitive host, induced a stronger positive geotaxis (presumably protecting gammarids from bird predation). In contrast, castration was almost total at the acanthella stage, with no significant variation in the intensity according to parasite maturation. Finally, no significant correlation was found between the intensity of behavioural changes and the intensity of castration. We discuss our results in relation with current views on the evolution of multidimensionality in PIPA.

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