Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite

2010

Competitive interactions between coinfecting parasites are expected to be strong when they affect transmission success. When transmission is enhanced by altering host behaviour, intraspecific conflict can lead to ‘coinfection exclusion’ by the first-in parasite or to a ‘sabotage’ of behavioural manipulation by the youngest noninfective parasite. We tested these hypotheses in the acanthocephalan parasite Pomphorhynchus laevis, reversing phototaxis in its intermediate host Gammarus pulex. No evidence was found for coinfection exclusion in gammarids sequentially exposed to infection. Behavioural manipulation was slightly weakened but not cancelled in gammarids infected with mixed larval stages…

Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation.

2009

Manipulation by parasites is a catchy concept that has been applied to a large range of phenotypic alterations brought about by parasites in their hosts. It has, for instance, been suggested that the carotenoid-based colour of acanthocephalan cystacanths is adaptive through increasing the conspicuousness of infected intermediate hosts and, hence, their vulnerability to appropriate final hosts such as fish predators. We revisited the evidence in favour of adaptive coloration of acanthocephalan parasites in relation to increased trophic transmission using the crustacean amphipodGammarus pulexand two species of acanthocephalans,Pomphorhynchus laevisandPolymorphus minutus. Both species show car…

Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the a…

2014

6 pages; International audience; Larvae of many trophically-transmitted parasites alter the behaviour of their intermediate host in ways that increase their probability of transmission to the next host in their life cycle. Before reaching a stage that is infective to the next host, parasite larvae may develop through several larval stages in the intermediate host that are not infective to the definitive host. Early predation at these stages results in parasite death, and it has recently been shown that non-infective larvae of some helminths decrease such risk by enhancing the anti-predator defences of the host, including decreased activity and increased sheltering. However, these behavioura…

Molecular markers for systematic identification and population genetics of the invasive Ponto-Caspian freshwater gammarid Dikerogammarus villosus (Cr…

2006

The Ponto-Caspian amphipod, Dikerogammarus villosus, is an invasive species of many European rivers. First, we show that size difference of nrDNA ITS1 allows discriminating D. villosus from Dikerogammarus bispinosus, a closely related but morphologically hardly distinguishable species. Second, we present two types of polymorphic markers for D. villosus, three microsatellites and two single nucleotide polymorphisms (SNPs) of mtDNA COI gene, which were scored by polymerase chain reaction-single strand conformational polymorphism (PCR-SSCP). These markers will be very useful in studying population genetics of D. villosus.

Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators.

2008

SUMMARYPhenotypic alterations induced by parasites in their intermediate hosts often result in enhanced trophic transmission to appropriate final hosts. However, such alterations may also increase the vulnerability of intermediate hosts to predation by non-host species. We studied the influence of both infection with 3 different acanthocephalan parasites (Pomphorhynchus laevis, P. tereticollis, and Polymorphus minutus) and the availability of refuges on the susceptibility of the amphipod Gammarus pulex to predation by 2 non-host predators in microcosms. Only infection with P. laevis increased the vulnerability of amphipods to predation by crayfish, Orconectes limosus. In contrast, in the ab…

Studying adaptive changes in the behaviour of infected hosts: a long and winding road

2005

Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: evidence for vertical transmission and posit…

2004

We investigated the prevalence, transmission mode and fitness effects of infections by obligatory intracellular, microsporidian parasites in the freshwater amphipod Gammarus roeseli. We found three different microsporidia species in this host, all using transovarial (vertical) transmission. All three coexist at different prevalences in two host populations, but bi-infected individuals were rarely found, suggesting no (or very little) horizontal transmission. It is predicted that vertically-transmitted parasites may exhibit sex-specific virulence in their hosts, or they may have either positive or neutral effects on host fitness. All three species differed in their transmission efficiency an…

The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pu…

2005

Acanthocephala are parasites with complex life cycles involving arthropod intermediate hosts and vertebrate final hosts. They use predation as a means of transmission, and some species have developed the ability to modify behaviour of their intermediate hosts to enhance the probability of ingestion by the definitive host. Knowledge of how a single parasite species is adapted to modify the behaviour of different intermediate host species is important for the understanding of parasitic transmission in host communities. In Burgundy, the freshwater amphipod crustaceans Gammarus pulex (native species) and Gammarus roeseli (eastern European invader) are both intermediate hosts for the acanthoceph…

Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species.

2007

The physiological mechanisms by which parasites with complex life cycles manipulate the behaviour of their intermediate hosts are still poorly understood. In Burgundy, eastern France, the acanthocephalan parasitePomphorhynchus laevisinverses reaction to light in its amphipod hostGammarus pulex, but not inGammarus roeseli, a recent invasive species. Here, we show that this difference in manipulation actually reflects a difference in the ability of the parasite to alter brain serotonergic (5-HT) activity of the two host species. Injection of 5-HT in uninfected individuals of both host species was sufficient to inverse reaction to light. However, a difference in brain 5-HT immunocytochemical s…

Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects.

2012

Summary Studies addressing the functional basis of parasitic manipulation suggest that alteration of the neuromodulatory system is a common feature of manipulated hosts. Screening of the neuromodulatory system has so far been carried out by performing ethopharmacological analysis, biochemical quantification of neurotransmitters and neuromodulators, and/or immunocytochemistry. Here, we review the advantages and limitations of such approaches through the analysis of case studies. We further address whether the analysis of candidate neuromodulatory systems fits the current view of manipulation as being multidimensional. The benefits in combining ethopharmacology with more recent molecular tool…

PROTECTION FIRST THEN FACILITATION: A MANIPULATIVE PARASITE MODULATES THE VULNERABILITY TO PREDATION OF ITS INTERMEDIATE HOST ACCORDING TO ITS OWN DE…

2011

Many trophically transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host's antipredatory defenses when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when noninfective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by n…

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence.

2010

10 pages; International audience; Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these…

Parasite-induced behavioral change: mechanisms.

2010

Animal behavior and parasitism are more tightly linked than commonly thought. One of the most astonishing phenomena in host–parasite antagonistic interactions is ‘host manipulation,’ that is, the ability of a parasite to alter the behavior of its host in ways that appear to increase parasite fitness at the expense of host fitness. The mechanisms by which a parasite hijacks the behavior of its host have been explored using ethopharmacological and immunocytochemical approaches or carrying out a large-scale proteomic study on manipulated host’s brain. These few mechanistic studies have confirmed both the complexity of host manipulation by parasites and the importance of understanding the molec…

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

2020

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta-analysis, focusing on a…

Intergenomic interactions affect female reproduction: evidence from introgression and inbreeding depression in a haplodiploid mite

2004

Nuclear and cytoplasmic genomes can coevolve antagonistically or harmoniously to affect fitness. One commonly used test for nuclear-cytoplasmic coadaptation relies on the breakup of coadapted gene complexes by introgression, potentially resulting in an increased frequency of nuclear alleles in deleterious interaction with an alien cytoplasm. We investigated the phenotypic effect of such genes on female reproduction in outbred and inbred introgressed lines of the haplodiploid mite Tetranychus urticae. Introgression changed female lifetime fecundity and increased male production, in ways suggesting a control of fecundity by nuclear genes. Conversely introgression reduced the fertilization rat…

Tracking paternal genes with DALP markers in a pseudoarrhenotokous reproductive system: biparental transmission but haplodiploid-like inheritance in …

2000

International audience; The complexity of some sexual reproductive systems in arthropods still leaves both their genetic and epigenetic determinism and their evolutionary significance poorly understood. Pseudoarrhenotoky is characterized by obligate fertilization and differential inactivation and/or elimination of paternal chromosomes in embryos that develop into males. Here, we investigate how the paternal genome is transmitted in a pseudoarrhenotokous mite, Neoseiulus californicus, using codominant genetic markers detected by DALP (direct amplification of length polymorphism). Transmission patterns of parental alleles through one and two generations are reported at four or five loci corre…

Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity

2006

Manipulative parasites can alter the phenotype of intermediate hosts in various ways. However, it is unclear whether such changes are just by-products of infection or adaptive and enhance transmission to the final host. Here, we show that the alteration of serotonergic activity is functionally linked to the alteration of specific behaviour in the amphipodGammarus pulexinfected with acanthocephalan parasites.Pomphorhynchus laevisand, to a lesser extent,Pomphorhynchus tereticollisaltered phototactism, but not geotactism, inG. pulex, whereas the reverse was true forPolymorphus minutus. Serotonin (5-hydroxytryptamine, 5-HT) injected to uninfectedG. pulexmimicked the altered phototactism, but ha…

Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers.

2002

International audience; The genetic structure of a greenhouse population of the mite Tetranychus urticae was studied by the analysis of five microsatellite loci. Genetic variation was compared during a crop season between periods of population foundation and rapid population increase and was investigated in two consecutive years. The population displayed significant heterozygote deficiency at all the sampling periods. However, inbreeding tended to decrease with increasing density (FIS coefficient between 0.13 and 0.25). No significant genetic differentiation between samples was found either at a spatial scale within the greenhouse or at a temporal scale between two growing seasons (FST betw…

Host-manipulation by parasites with complex life cycles: adaptive or not?

2010

7 pages; International audience; The effect of host manipulation by parasites on trophic transmission to final hosts remains unclear. The transmission benefits gained by manipulative parasites are difficult to assess, and evidence for a causal link between manipulation and trophic transmission is missing. In addition, infected intermediate hosts can also be more vulnerable to predation by nonhosts, whereas recent theoretical advances indicate that the evolution of host manipulation does not require increased specificity in trophic transmission. We propose that a deeper consideration of the evolution of complex life cycles in helminth parasites might provide a different perspective on the ev…

Contrasting effects ofWolbachiaon cytoplasmic incompatibility and fecundity in the haplodiploid miteTetranychus urticae

2002

Recent studies on Wolbachia-induced incompatibility in haplodiploid insects and mites have revealed a diversity of cytoplasmic incompatibility (CI) patterns among host species. Here, we report intraspecific diversity in CI expression among four strains of the arrhenotokous mite Tetranychus urticae and in T. turkestani. Variability of CI expression within T. urticae ranged from no CI to complete CI, and included either female embryonic mortality or male conversion types of CI. A fecundity cost attributed to the infection with the high-CI Wolbachia strain was the highest ever recorded for Wolbachia (−80 to −100% decrease). Sequence polymorphism at a 550-bp-portion of Wolbachia wsp gene reveal…

Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with …

2012

Summary 1.Many parasites with complex life cycles critically rely on trophic transmission to pass from an intermediate host to a final host. Parasite-induced behavioural alterations in intermediate hosts are often supposed to be adaptive through increasing the susceptibility of intermediate hosts to predation by final hosts. However, the evidence is so far only correlational, and direct evidence for a causal link between one single behavioural alteration and increased trophic transmission is still missing. 2.Here, we addressed, for the first time, the relationship between increased vulnerability to fish predation and altered photophobia in an amphipod, Gammarus pulex, infected with a fish a…

Shaping the antipredator strategy: flexibility, consistency, and behavioral correlations under varying predation threat

2014

9 pages; International audience; Recent ecological and evolutionary research emphasizes the importance of adaptive trait integration. For instance, antipredator defenses are built up of several morphological and behavioral components in many species, yet their functional relationships are still poorly documented. Using field-collected freshwater crustaceans Gammarus fossarum in a within-subject design, we investigated the flexibility and consistency of refuge use, photophobia, and exploration behavior as well as their associations, quantified both when predation risk was absent or artificially simulated. In agreement with the "threat-sensitivity" hypothesis, both refuge use and photophobia …

Modulatory effects of the serotonergic and histaminergic systems on reaction to light in the crustacean Gammarus pulex

2013

Serotonin modulates reaction to light in many animals. In the freshwater amphipod Gammarus pulex, exogenous administration of serotonin induces a transient reversal of photic behaviour from strong photophobia to photophily. We have elucidated further the neuromodulation of photic behaviour in G. pulex by using in vivo pharmacology and behavioural testing. Using several mammalian 5-HT receptor antagonists and agonists, we provide evidence for a role of serotonin receptors in the 5-HT-dependent regulation of G. pulex photic behaviour, possibly involving 5-HTR2 subtype. Serotonin-induced photophily was blocked by the 5-HT receptor antagonists, mianserin, cyproheptadine, and ritanserin, but not…

Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts?

2006

Phylogenetically unrelated parasites often increase the chances of their transmission by inducing similar phenotypic changes in their hosts. However, it is not known whether these convergent strategies rely on the same biochemical precursors. In this paper, we explored such aspects by studying two gammarid species ( Gammarus insensibilis and Gammarus pulex ; Crustacea: Amphipoda: Gammaridae) serving as intermediate hosts in the life cycle of two distantly related parasites: the trematode, Microphallus papillorobustus and the acanthocephalan, Polymorphus minutus . Both these parasite species are known to manipulate the behaviour of their amphipod hosts, bringing them towards the water surfa…

Carotenoids of two freshwater amphipod species (Gammarus pulex and G. roeseli) and their common acanthocephalan parasite Polymorphus minutus

2004

Carotenoid compositions of two freshwater Gammarus species (Crustacea: Amphipoda) and of their common acanthocephalan parasite Polymorphus minutus were characterized. The effect of carotenoid uptake by the parasite was addressed by comparing the carotenoid content of uninfected and infected female hosts. Using high-pressure liquid chromatography (HPLC), co-chromatography of reference pigments and electron ionization mass spectrometry of collected HPLC fractions (EI-MS), several xanthophylls and non-polar compounds were identified. Seven kinds of carotenoids, mainly xanthophylls, were identified in gammarids. Astaxanthin was predominant, amounting to 40 wt.% of total carotenoid in both uninf…

A minimalist macroparasite diversity in the round goby of the Upper Rhine reduced to an exotic acanthocephalan lineage.

2018

AbstractThe round goby, Neogobius melanostomus, is a Ponto-Caspian fish considered as an invasive species in a wide range of aquatic ecosystems. To understand the role that parasites may play in its successful invasion across Western Europe, we investigated the parasitic diversity of the round goby along its invasion corridor, from the Danube to the Upper Rhine rivers, using data from literature and a molecular barcoding approach, respectively. Among 1666 parasites extracted from 179 gobies of the Upper Rhine, all of the 248 parasites barcoded on the c oxidase subunit I gene were identified as Pomphorhynchus laevis. This lack of macroparasite diversity was interpreted as a loss of parasites…

Pigmentation polymorphism in the invasive amphipod Dikerogammarus villosus : some insights into its maintenance

2004

Dikerogammarus villosus, a freshwater invasive amphipod, exhibits conspicuous pigmentation polymorphism. This polymorphism is documented in two recently colonized areas, the Saand Moselle rivers (north-eastern France), and some of the mechanisms by which pigmentation polymorphism can arise and be maintained are addressed. Body size, reproductive status, fecundity and mate choice are compared among morphs of D. villosus in field samples collected in summer 2001. Body size and female gonad developmental stage were comparable among the different morphs, suggesting that polymorphism is not the result of changes in pigmentation with age or moult- cycle. Fecundity and reproductive status (paired …

Multidimensionality in host manipulation mimicked by serotonin injection.

2014

Manipulative parasites often alter the phenotype of their hosts along multiple dimensions. ‘Multidimensionality’ in host manipulation could consist in the simultaneous alteration of several physiological pathways independently of one another, or proceed from the disruption of some key physiological parameter, followed by a cascade of effects. We compared multidimensionality in ‘host manipulation’ between two closely related amphipods, Gammarus fossarum and Gammarus pulex, naturally and experimentally infected with Pomphorhynchus laevis (Acanthocephala), respectively. To that end, we calculated in each host–parasite association the effect size of the difference between infected and uninfect…

Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod.

2007

7 pages; International audience; According to the 'parasitic manipulation hypothesis', phenotypic changes induced by parasites in their intermediate hosts are effective means of increasing trophic transmission to final hosts. One obvious prediction, although seldom tested, is that increased vulnerability of infected prey to an appropriate predator should be achieved by the parasite altering the anti-predator behaviour of its intermediate host. In this study, we tested this prediction using the fish acanthocephalan Pomphorhynchus tereticollis and the freshwater amphipod Gammarus pulex. Firstly, we estimated the relative vulnerability of infected and uninfected gammarids to predation by the b…

Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects.

2012

SummaryIn most cases, parasites alter more than one dimension in their host phenotype. Although multidimensionality in parasite-induced phenotypic alterations (PIPAs) seems to be the rule, it has started to be addressed only recently. Here, we critically review some of the problems associated with the definition, quantification and interpretation of multidimensionality in PIPAs. In particular, we confront ultimate and proximate accounts, and evaluate their own limitations. We end up by introducing several suggestions for the development of future research, including some practical guidelines for the quantitative analysis of multidimensionality in PIPAs.

Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate …

2011

9 pages; International audience; Few endoparasite species are pigmented. Acanthocephalans are an exception however, with several species being characterised by yellow to orange colouration both at the immature (cystacanth) and adult stages. However, the functional and adaptive significance of carotenoid-based colourations in acanthocephalans remains unclear. One possibility is that the carotenoid content of acanthocephalan cystacanths acts as a protective device against ultra-violet radiation (UVR) passing through the translucent cuticle of their crustacean hosts. Indeed, acanthocephalans often bring about behavioural changes in their aquatic intermediate hosts that can increase their expos…

Cooperation and conflict in host manipulation: interactions among macro-parasites and micro-organisms.

2014

10 pages; International audience; Several parasite species are known to manipulate the phenotype of their hosts in ways that enhance their own transmission. Co-occurrence of manipulative parasites, belonging to the same species or to more than one species, in a single host has been regularly observed. Little is known, however, on interactions between co-occurring manipulative parasites with same or different transmission routes. Several models addressing this problem have provided predictions on how cooperation and conflict between parasites could emerge from multiple infections. Here, we review the empirical evidence in favor of the existence of synergistic or antagonistic interactions bet…

Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host

2007

7 pages; International audience; Fish acanthocephalans can modify the antipredator behaviour of their intermediate hosts in response to cues from fish predators. However, it is still unclear whether such behavioural changes are adaptive, or are just the consequence of infection. We addressed this question through studying two acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus, and their intermediate host, the amphipod Gammarus pulex. Pomphorhynchus laevis completes its cycle in a freshwater fish, whereas P. minutus exploits waterbirds as final hosts.We first assessed vulnerability of infected and uninfected gammarids to predation by bullheads, Cottus gobio. Pomphorhynchus laevi…

External Influences on Invertebrate Brain Histamine and Related Compounds via an Automated Derivatization Method for Capillary Electrophoresis.

2017

8 pages; International audience; Histamine has been shown to modulate visual system and photic behavior in arthropods. However, few methods are available for the direct quantification of histamine and its precursor and metabolites in arthropod brain. In this work, a method for the separation of histamine, its precursor histidine, and its metabolite N-methyl-histamine from brain extracts of a freshwater crustacean has been developed using capillary electrophoresis with laser-induced fluorescence detection. Molecules were tagged on their primary amine function with naphthalene-2,3-dicarboxaldehyde, but derivatized histamine and N-methyl-histamine exhibited poor stability in contrast to deriva…

Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation.

2007

9 pages; International audience; Parasites relying on trophic transmission to complete their life cycles often induce modifications of their host's behavior in ways that may increase their susceptibility to predation by final hosts. These modifications have often been interpreted as parasite adaptations, but very few studies have demonstrated that host manipulation has fitness benefits for the parasite. The aim of the present study was to address the adaptive significance of parasite manipulation by coupling observations of behavioral manipulation to estimates of trophic transmission to the definitive host in the natural environment. We show that the acanthocephalan parasite Pomphorhynchus …

Data from: Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to…

2011

Many trophically-transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host’s anti-predatory defences when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when non-infective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by…

Data from: Multidimensionality in host manipulation mimicked by serotonin injection

2014

Manipulative parasites often alter the phenotype of their hosts along multiple dimensions. ‘Multidimensionality’ in host manipulation could consist in the simultaneous alteration of several physiological pathways independently of one another, or proceed from the disruption of some key physiological parameter, followed by a cascade of effects. We compared multidimensionality in ‘host manipulation’ between two closely related amphipods, Gammarus fossarum and Gammarus pulex, naturally and experimentally infected with Pomphorhynchus laevis (Acanthocephala), respectively. To that end, we calculated in each host–parasite association the effect size of the difference between infected and uninfecte…