Evolutionary routes leading to host manipulation by parasites

18 pages; International audience

Widespread vertical transmission and associated host sex–ratio distortion within the eukaryotic phylum Microspora

Vertical transmission (VT) and associated manipulation of host reproduction are widely reported among prokaryotic endosymbionts. Here, we present evidence for widespread use of VT and associated sex-ratio distortion in a eukaryotic phylum. The Microspora are an unusual and diverse group of eukaryotic parasites that infect all animal phyla. Following our initial description of a microsporidian that feminizes its crustacean host, we survey the diversity and distribution of VT within the Microspora. We find that vertically transmitted microsporidia are ubiquitous in the amphipod hosts sampled and that they are also diverse, with 11 species of microsporidia detected within 16 host species. We f…

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

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…

The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies

In many natural populations, hosts are found to be infected by more than one parasite species. When these parasites have different host exploitation strategies and transmission modes, a conflict among them may arise. Such a conflict may reduce the success of both parasites, but could work to the benefit of the host. For example, the less-virulent parasite may protect the host against the more-virulent competitor. We examine this conflict using the waterflea Daphnia magna and two of its sympatric parasites: the blood-infecting bacterium Pasteuria ramosa that transmits horizontally and the intracellular microsporidium Octosporea bayeri that can concurrently transmit horizontally and verticall…

Isolation and characterization of 8 microsatellite loci for the "killer shrimp'', an invasive Ponto-Caspian amphipod Dikerogammarus villosus (Crustacea: Amphipoda).

5 pages; International audience; Dikerogammarus villosus is a freshwater amphipod of the Ponto-Caspian origin recognized as one of the 100 worst alien species in Europe, having negative impact on biodiversity and functioning of the invaded aquatic ecosystems. The species has a wide ecophysiological tolerance and during the last 20 years it has rapidly spread throughout European inland waters. In consequence, it presents a major conservation management problem. We describe eight polymorphic microsatellite loci developed for D. villosus by combining a biotin-enrichment protocol and new generation 454GS-FLX Titanium pyrosequencing technology. When genotyped in 64 individuals from two locations…

Variation and covariation in infectivity, virulence and immunodepression in the host-parasite association Gammarus pulex-Pomphorhynchus laevis.

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis , in infecting and in immunodepressing its amphipod host, Gammarus pulex . We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infecti…

Interaction between Medicago truncatula and Pseudomonas fluorescens: evaluation of costs and benefits across an elevated atmospheric CO2.

10 pages; International audience; Soil microorganisms play a key role in both plants nutrition and health. Their relation with plant varies from mutualism to parasitism, according to the balance of costs and benefits for the two partners of the interaction. These interactions involved the liberation of plant organic compounds via rhizodeposition. Modification of atmospheric CO2 concentration may affect rhizodeposition and as a consequence trophic interactions that bind plants and microorganisms. Positive effect of elevated CO2 on plants are rather well known but consequences for micoorganisms and their interactions with plants are still poorly understood. A gnotobiotic system has been devel…

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

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…

Parasite-induced suppression of aggregation under predation risk in a freshwater amphipod

a b s t r a c t Recent findings suggest that grouping with conspecifics is part of the behavioural defences developed by amphipod crustaceans to face predation risk by fish. Amphipods commonly serve as intermediate hosts for trophically transmitted parasites. These parasites are known for their ability to alter intermediate host phenotype in a way that promotes predation by definitive hosts, where they reproduce. If aggregation in amphipods dilutes the risk to be preyed on by fish, then it may dilute the probability of transmission for the parasite using fish as definitive hosts. Using experimental infections, we tested whether infection with the fish acanthocephalan Pomphorhynchus laevis a…

Is metal accumulation in Pomphorhynchus laevis dependent on parasite sex or infrapopulation size?

SUMMARYConcentrations of the elements As, Cd, Co, Cu, Fe, Mn, Mo, Ni, Pb, Sn, V, Zn were analysed by inductively coupled plasma mass spectrometry (ICP-MS) in the acanthocephalan Pomphorhynchus laevis and its fish host Barbus barbus. A total of 27 barbels were collected from the Danube River in autumn 2006 close to the town Kozloduy (685 river kilometer) on the Bulgarian river bank. Fish were divided into 3 groups. According to their P. laevis infrapopulation size hosts were considered as heavily infected (>100 worms per fish) and lightly infected (<20 worms per fish). The third group was used to compare heavy metal concentrations between male and female P. laevis. The 5 elements As, C…

Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: potential consequences

Non-indigenous species are increasingly recognized as altering local com- munities in newly colonized areas. In some north European freshwater systems, the Ponto-Caspian invasive crustacean Dikerogammarus villosus (Amphipoda) is im- plicated to have such an effect, with general monitoring of its progress and general im- pact required. The present study contributes to this monitoring. D. villosus was ob- served in 2003 in all the major French rivers prospected (i.e. Rhine, Meuse, Moselle, Sao ne, Rho ne, Seine, and Loire), a European region previously overlooked for its co- lonization. This species was also detected in some tributaries of the rivers Sao ne and Seine, and in Geneva Lake. The …

Variation in the immune state of Gammarus pulex (Crustacea, Amphipoda) according to temperature: are extreme temperatures a stress?

9 pages; International audience; Temperature is known to impact host-parasite interactions in various ways. Such effects are often regarded as the consequence of the increased metabolism of parasites with increasing temperature. However, the effect of temperature on hosts' immune system could also be a determinant. Here we assessed the influence of temperature on the immunocompetence of the crustacean amphipod Gammarus pulex. Amphipods play a key ecological role in freshwater ecosystems that can be altered by several parasites. We investigated the consequences of three weeks of acclimatization at four temperatures (from 9 °C to 17 °C) on different immunological parameters. Temperature influ…

A co-invasive microsporidian parasite that reduces the predatory behaviour of its host Dikerogammarus villosus (Crustacea, Amphipoda).

SUMMARYParasites are known to affect the predatory behaviour or diet of their hosts. In relation to biological invasions, parasites may significantly influence the invasiveness of the host population and/or mediate the relationships between the invader and the invaded community. Dikerogammarus villosus, a recently introduced species, has had a major impact in European rivers. Notably, its high position in trophic web and high predatory behaviour, have both facilitated its invasive success, and affected other macroinvertebrate taxa in colonized habitats. The intracellular parasite Cucumispora dikerogammari, specific to D. villosus, has successfully dispersed together with this amphipod. Data…

Intraspecific variability in host manipulation by parasites

8 pages; International audience; Manipulative parasites have the capacity to alter a broad range of phenotypic traits in their hosts, extending from colour, morphology and behaviour. While significant attention has been devoted to describing the diversity of host manipulation among parasite clades, and testing the adaptive value of phenotypic traits that can be manipulated, there is increasing evidence that variation exists in the frequency and intensity of the changes displayed by parasitized individuals within single host-manipulative parasite systems. Such variability occurs within individuals, between individuals of a same population, and across populations. Here we review the non-genet…

Infection by a vertically-transmitted microsporidian parasite is associated with a female-biased sex ratio and survival advantage in the amphipod Gammarus roeseli

SUMMARYVertically transmitted parasites may have positive, neutral or negative effects on host fitness, and are also predicted to exhibit sex-specific virulence to increase the proportion or fitness of the transmitting sex. We investigated these predictions in a study on the survival and sex ratio of offspring of the amphipod Gammarus roeseli from females infected by the vertically transmitted microsporidia Nosema granulosis. We found, to our knowledge, the first evidence for a positive relationship between N. granulosis infection and host survival. Infection was associated with sex ratio distortion, not by male-killing, but probably by parasite-induced feminization of putative G. roeseli m…

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 December 2009-31 January 2010

4 pages; International audience; This article documents the addition of 220 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Allanblackia floribunda, Amblyraja radiata, Bactrocera cucurbitae, Brachycaudus helichrysi, Calopogonium mucunoides, Dissodactylus primitivus, Elodea canadensis, Ephydatia fluviatilis, Galapaganus howdenae howdenae, Hoplostethus atlanticus, Ischnura elegans, Larimichthys polyactis, Opheodrys vernalis, Pelteobagrus fulvidraco, Phragmidium violaceum, Pistacia vera, and Thunnus thynnus. These loci were cross-tested on the following species: Allanblackia gabonensis, Allanblackia stanerana, Neoceratitis …

Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: evidence for vertical transmission and positive effect on reproduction

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…

Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes.

16 pages; International audience; Freshwater amphipods Gammarus fossarum and Gammarus pulex are widespread in Europe, with some evidence of cryptic diversity in the former. We used DNA barcoding to assess genetic diversity within and among amphipod populations and examined mate discrimination and pre-copulatory pair formation between genetically divergent individuals. Eight distinct G. fossarum and four distinct G. pulex molecular operational taxonomic units (MOTUs) were detected. Among the 33 amphipod populations sampled, 11 contained a single MOTU, 11 had two and 11 were composed of three sympatric MOTUs. Genetic divergences between sympatric MOTUs (G. fossarum and G. pulex MOTUs combined…

Identifying a key host in an acanthocephalan-amphipod system.

SUMMARYTrophically transmitted parasites may use multiple intermediate hosts, some of which may be ‘key-hosts’, i.e. contributing significantly more to the completion of the parasite life cycle, while others may be ‘sink hosts’ with a poor contribution to parasite transmission. Gammarus fossarum and Gammarus roeseli are sympatric crustaceans used as intermediate hosts by the acanthocephalan Pomphorhynchus laevis. Gammarus roeseli suffers higher field prevalence and is less sensitive to parasite behavioural manipulation and to predation by definitive hosts. However, no data are available on between-host differences in susceptibility to P. laevis infection, making it difficult to untangle the…

The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli

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…

Variation in the risk of being wounded: an overlooked factor in studies of invertebrate immune function?

In invertebrates, wounding can trigger an immune response, and will often expose organisms to parasites and pathogens. Here we show that in the amphipod Gammarus pulex, wounding abundance is negatively correlated with PhenolOxidase activity (a major component of the invertebrate immune response), and that the occurrence and abundance of wounding is extremely high and varies significantly between five natural populations. In some populations the prevalence and abundance of wounds also varied between sexes. Given that, using and maintaining an efficient immune system is costly, we suggest that the frequency of wounding may be an important selective pressure influencing an organism's optimal i…

Cucumispora dikerogammari n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers.

SUMMARYDikerogammarus villosusis an invasive amphipod that recently colonized the main rivers of Central and Western Europe. Two frequent microsporidian parasites were previously detected in this species, but their taxonomic status was unclear. Here we present ultrastructural and molecular data indicating that these two parasites are in fact a single microsporidian species. This parasite shares numerous characteristics ofNosemaspp. It forms elongate spores (cucumiform), developing in direct contact with host cell cytoplasm; all developmental stages are diplokaryotic and the life cycle is monomorphic with disporoblastic sporogony. Initially this parasite was described asNosema dikerogammariO…

Spines and behaviour as defences against fish predators in an invasive freshwater amphipod.

7 pages; International audience; Selective predation may be an important proximate cause of the success or failure of invader species. Gammarus roeseli is an invasive amphipod, for which the causes of establishment in rivers where the native species, Gammarus pulex, predominates remain unstudied. Freshwater amphipods are important prey for numerous fish predators, but empirical evidence of lower predation rates on exotic prey is scarce. In laboratory experiments, we compared the susceptibility of G. pulex and G. roeseli to fish predation, determined the mechanisms influencing prey selection, and studied the interaction between behavioural and morphological defences. Fish predators (brown tr…

Chromosome-scale assembly of the yellow mealworm genome

Background: The yellow mealworm beetle, Tenebrio molitor, is a promising alternative protein source for animal and human nutrition and its farming involves relatively low environmental costs. For these reasons, its industrial scale production started this century. However, to optimize and breed sustainable new T. molitor lines, the access to its genome remains essential. Methods: By combining Oxford Nanopore and Illumina Hi-C data, we constructed a high-quality chromosome-scale assembly of T. molitor. Then, we combined RNA-seq data and available coleoptera proteomes for gene prediction with GMOVE. Results: We produced a high-quality genome with a N50 = 21.9Mb with a completeness of 99.5% an…

Ectosymbiosis associated with cidaroids (Echinodermata: Echinoidea) promotes benthic colonization of the seafloor in the Larsen Embayments, Western Antarctica

7 pages; International audience; Ice-shelf collapses in the Larsen A and B embayments along the Weddell side of the Antarctic Peninsula resulted in new open-water areas that are likely reorganizing benthic communities. It is a natural laboratory to assess colonization of the sea bottom under new conditions. We tested the hypothesis that the epibionts associated to cidaroid echinoids could promote or enhance the colonization of hard surfaces. In fact, being vagile, cidaroids might improve dispersal capabilities of the sessile animals that are attached to their spines, e.g., promoting the colonization of areas where the fauna has been eradicated by iceberg scouring. If this hypothesis is corr…

Chemical host detection and differential attraction in a parasitic pea crab infecting two echinoids

Mechanisms of host detection and host choice are important for mobile parasites or symbionts that frequently move among host individuals. The parasitic pea crab Dissodactylus primitivus is an ectoparasite exploiting asymmetrically two spatangoid echinoid hosts, Meoma ventricosa and Plagiobrissus grandis. The entire life cycle takes place on M. ventricosa, while only adults colonize P. grandis, the host where female's fecundity is the greatest. Dissodactylus primitivus frequently exhibits host-switching, a behaviour that raises the question of host detection. To test if adult crabs are able to detect potential hosts and are attracted to the host where their fitness is greater, crab olfactory…

Ectosymbiosis is a critical factor in the local benthic biodiversity of the Antarctic deep sea.

10 pages; International audience; In deep-sea benthic environments, competition for hard substrates is a critical factor in the distribution and diversity of organisms. In this context, the occurrence of biotic substrates in addition to mineral substrates may change the characteristics of sessile fauna. We tested this hypothesis at different localities of the Weddell Sea (Antarctica) by studying the diversity of ectosymbionts living on the spines of cidaroids (echinoids). The presence of cidaroids promoted a higher total specific richness and increased sessile species abundance, but did not change the diversity. Analyses of species distribution suggested that the cidaroids are a favourable …

Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan-amphipod system.

8 pages; International audience; Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co-variati…

Out of the Black Sea: phylogeography of the invasive killer shrimp Dikerogammarus villosus across Europe.

20 pages; International audience; The amphipod Dikerogammarus villosus has colonized most of the European main inland water bodies in less than 20 years, having deteriorating effect on the local benthic communities. Our aim was to reveal the species phylogeography in the native Black Sea area, to define the source populations for the colonization routes in continental Europe and for the newly established UK populations. We tested for the loss of genetic diversity between source and invasive populations as well as along invasion route. We tested also for isolation by distance. Thirty three native and invasive populations were genotyped for mtDNA (COI, 16S) and seven polymorphic nuclear micro…

A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod.

A number of parasites are vertically transmitted to new host generations via female eggs. In such cases, host reproduction is an intimate component of parasite fitness and no cost of the infection on host reproduction is expected to evolve. A number of these parasites distort host sex ratios towards females, thereby increasing either parasite fitness or the proportion of the host that transmit the parasite. In terrestrial isopods (woodlice), Wolbachia bacteria are responsible for sex reversion and female-biased sex ratios, changing genetic males into functional neo-females. Although sex ratio distortion is a powerful means for parasites to increase in frequency in host populations, it also …

Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation.

9 pages; International audience; Parasite survival in hosts mainly depends on the capacity to circumvent the host immune response. Acanthocephalan infections in gammarids are linked with decreased activity of the prophenoloxidase (ProPO) system, suggesting an active immunosuppression process. Nevertheless, experimental evidence for this hypothesis is lacking: whether these parasites affect several immune pathways is unknown and the consequences of such immune change have not been investigated. In particular, the consequences for other pathogens are not known; neither are the links with other parasite-induced manipulations of the host. Firstly, using experimental infections of Pomphorhynchus…

Biodiversity of three representative groups of the Antarctic zoobenthos: comparative structure, distribution and function.

95 pages

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

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…

Invasion de Dikerogammarus villosus (Crustacé, Amphipode) dans les eaux continentales françaises : dynamiques et conséquences

National audience

Combining molecular microbial ecology with ecophysiology and plant genetics for a better understanding of plant-microbial communities' interactions in the rhizosphere.

18 pages; International audience

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

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…

Highly contrasted population genetic structures in a host-parasite pair in the Caribbean Sea.

Evolution and population genetic structure of marine species across the Caribbean Sea are shaped by two complex factors: the geological history and the present pattern of marine currents. Characterizing and comparing the genetic structures of codistributed species, such as host–parasite associations, allow discriminating the relative importance of environmental factors and life history traits that influenced gene flow and demographic events. Using microsatellite and Cytochrome Oxidase I markers, we investigated if a host–parasite pair (the heart urchin Meoma ventricosa and its parasitic pea crab Dissodactylus primitivus) exhibits comparable population genetic structures in the Caribbean Sea…

Hermaphrodisme et transsexualité.

50 pages

Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna.

12 pages; International audience; Invasive species may introduce novel pathogens to a colonised area. Most of the time emerging pathogens are detected a posteriori, but recognition of a priori emergence of an invasive disease by host shift may be useful for predictive purposes. Here, we studied if the microsporidian parasite Cucumispora dikerogammari infecting the invasive Ponto-Caspian amphipod Dikerogammarus villosus, has the potential to become an emergent disease in invaded rivers in Western and Central Europe. We first showed that this parasite decreases the survival of D. villosus in the later stages of infection development. However, the host reproduces earlier in response to the inf…

Host manipulation in the face of environmental changes: Ecological consequences

Several parasite species, particularly those having complex life-cycles, are known to induce phenotypic alterations in their hosts. Most often, such alterations appear to increase the fitness of the parasites at the expense of that of their hosts, a phenomenon known as “host manipulation”. Host manipulation can have important consequences, ranging from host population dynamics to ecosystem engineering. So far, the importance of environmental changes for host manipulation has received little attention. However, because manipulative parasites are embedded in complex systems, with many interacting components, changes in the environment are likely to affect those systems in various ways. Here, …

Breeding birds in Burgundy, 2006-2018.

How do Wolbachia Symbionts Increase the Proportion of Females in Their Hosts?

Effect of Multiple Parasitic Infections on the Tolerance to Pollutant Contamination

8 pages; International audience; The horizontally-transmitted acanthocephalan parasite Polymorphus minutus and the vertically-transmitted microsporidian parasite Dictyocoela roeselum have both been shown to influence on the antitoxic responses of mono-infected Gammarus roeseli exposed to cadmium. The present study investigates the effect of this co-infection on the antitoxic defence responses of naturally infected females exposed to cadmium stress. Our results revealed that, depending on the cadmium dose, bi-infection induced only slight, significant increased cell damage in G. roeseli as compared to non-infection. In addition, the antitoxic defence pattern of cadmium-exposed bi-infected ho…

A manipulative parasite increasing an antipredator response decreases its vulnerability to a nonhost predator.

8 pages; International audience; Trophically transmitted parasites have to deal with the antipredator adaptations of their intermediate hosts. Some of these parasites induce behavioural changes in their intermediate hosts that make them more vulnerable to predation by definitive hosts. However, the adaptiveness of behavioural manipulation also depends on the probability of being eaten by a nonhost predator. Parasites might therefore try to use specific antipredator responses of intermediate hosts to avoid this dead end. We tested this hypothesis using the acanthocephalan Polymorphus minutus and its intermediate amphipod host, Gammarus roeseli. In their natural habitat, uninfected G. roeseli…

Cd-resistance in field Gammarus populations: genetic adaptation, transgenerational effect, or selection of phylogenetic cryptic lineages?

International audience; We have recently identified a field population of the crustacean Gammarus fossarum historically-exposed (geochemical background) to cadmium (Cd) that exhibits a resistance transmissible to offspring. This population constitutes a good case study to investigate mechanisms underlying population’s resistance to long-term exposure to contamination that are of deep concern for ERA, especially in the field. In order to gain insights into the determinism of the Cd-resistance observed in this historically-exposed population, we applied quantitative genetic protocols both in two Cd-naive populations and in the resistant one. In addition, because G. fossarum is known to consti…

Larval size in acanthocephalan parasites : Influence of intraspecific competition and effects on intermediate host behavioural changes

Abstract Background Parasites often face a trade-off between exploitation of host resources and transmission probabilities to the next host. In helminths, larval growth, a major component of adult parasite fitness, is linked to exploitation of intermediate host resources and is influenced by the presence of co-infecting conspecifics. In manipulative parasites, larval growth strategy could also interact with their ability to alter intermediate host phenotype and influence parasite transmission. Methods We used experimental infections of Gammarus pulex by Pomphorhynchus laevis (Acanthocephala), to investigate larval size effects on host behavioural manipulation among different parasite sibshi…

Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda)

Acanthocephalan parasites are known to alter the reproductive biology and physiology of their hosts in various ways. In this study we investigated the influence of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on the fecundity and pairing success of female Gammarus pulex. The results show that P. laevis and P. minutus affect female intermediate host reproduction in different ways. Females infected with P. minutus were totally castrated, whereas those infected with P. laevis only showed reduced fecundity. The oocytes of P. laevis-infected females showed a similar structure to those of uninfected females, although infected females had a higher proportion of ooc…

Managing biotic interactions for ecological intensification of agroecosystems.

9 pages; International audience; Agriculture faces the challenge of increasing food production while simultaneously reducing the use of inputs and delivering other ecosystem services. Ecological intensification of agriculture is a paradigm shift, which has recently been proposed to meet such challenges through the manipulation of biotic interactions. While this approach opens up new possibilities, there are many constraints related to the complexity of agroecosystems that make it difficult to implement. Future advances, which are essential to guide agricultural policy, require an eco-evolutionary framework to ensure that ecological intensification is beneficial in the long term.

Microsporidia parasites disrupt the responses to cadmium exposure in a gammarid.

7 pages; International audience; Microsporidia parasites are commonly found in amphipods, where they are often asymptomatic, vertically-transmitted and have several effects on host sexuality and behaviour. As amphipods are often used as models in ecotoxicological studies, we investigated the effect of microsporidian infections on energy reserves and defence capacities of Gammarus roeseli under cadmium stress. Only females were infected by two microsporidia parasites: Dictyocoela roeselum or Dictyocoela muelleri. In physiological conditions, microsporidia had no major effect on energy reserves and defence capacities of G. roeseli, while under cadmium exposure, energy reserves and antioxidant…

Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite–induced excess of females?

Numerous animals are known to harbour intracytoplasmic symbionts that gain transmission to a new host generation via female eggs and not male sperm. Bacteria of the genus Wolbachia are a typical example. They infect a large range of arthropod species and manipulate host reproduction in several ways. In terrestrial isopods (woodlice), Wolbachia are responsible for converting males into females (feminization (F)) in some species, or for infertility in certain host crosses in other species (cytoplasmic incompatibility (CI)). Wolbachia with the F phenotype impose a strong excess of females on their host populations, while Wolbachia expressing CI do not. Here, we test the possibility that male m…

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN-INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative eff…

Condition-dependent ecdysis and immunocompetence in the amphipod crustacean, Gammarus pulex.

The exoskeleton of arthropods forms an efficient protection against pathogens, but this first line of defence is periodically weakened during ecdysis, increasing the opportunity for surrounding pathogens to invade the body cavity. Since the richness of pathogens in the environment can be spatially and temporally variable, arthropods may have a fitness advantage in moulting in a place and time of low infection risk. Consistent with this hypothesis, we found that the amphipod crustacean, Gammarus pulex , exhibits temporal adjustment of the moult cycle in response to elevated risks of infection. Interestingly, this phenomenon is variable between two populations and independent of levels of im…

The killer shrimp, Dikerogammarus villosus, invading European Alpine lakes: a single main source but independent founder events with an overall loss of genetic diversity.

16 pages; International audience; 1. The effects of biological invasions are generally more detrimental in isolated ecosystems than in the interconnected ones and freshwater lakes appear to be particularly fragile. The Ponto-Caspian freshwater amphipod Dikerogammarus villosus (Pontogammaridae), also known as the killer shrimp, is a highly invasive species that can have significant ecological impacts on receiving ecosystems. It has colonised most of the European main inland waterbodies, including at least 12 lakes in the Alps – an area of high conservational priority and, at the same time, heavily affected by anthropogenic changes. Particularly, overland translocations of boats among tourist…

Genetic evidence confirms polygamous mating system in a crustacean parasite with multiple hosts.

Mating systems are diverse in animals, notably in crustaceans, but can be inferred from a limited set of parameters. Baeza and Thiel (2007) proposed a model predicting mating systems of symbiotic crustaceans with three host characteristics and the risk of predation. These authors proposed five mating systems, ranging from monogamy to polygynandry (where multiple mating occurs for both genders). Using microsatellite loci, we tested the putatively mating system of the ectoparasite crab Dissodactylus primitivus. We determined the mating frequencies of males and females, parentage assignment (COLONY & GERUD software) as well as the contents of female spermathecae. Our results are globally consi…

Costs-benfits trade-off in the intercation between Medicago truncatula and Pseudomonas fluorescens C7R12 across atmospheric carbon dioxide modulation

The interactions between plants and soil microorganisms are mainly based on trophic relationships. The compounds exchanged represent cost for the organism produces them but a benefit for the one who receive those compounds. A mutualistic relation leads to stability in the cost-benefit balance resulting from a co-evolution between the two organisms. The cost corresponding for the release of carbon compounds by the plant would be offset by benefits in return corresponding for the activities of microorganisms that use them. We tested by an experimental way the effect of CO2 concentration on the interaction between M. truncatula and the bacterium P. fluorescens C7R12. The results allowed a best…

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, G…

Conflict between co-occurring parasites as a confounding factor in manipulation studies?

In their review, Thomas et al. (2005) highlight that, in cases where multiple infections occur in the same intermediate host individual, parasitic manipulation may be the result of not just a single parasite, but may be the cumulative effect of infection by two or more manipulating parasites. Such parasites may be in conflict when they share the same intermediate host but have different final hosts: they may manipulate the host in different ways in order to effect their different transmission p T c r s t s

Extension rapide de l'aire de répartition de Dikerogammarus villosus (Crustacé, Amphipode) en France : Causes et conséquences

International audience

Is the host or the parasite the most locally adapted in an amphipod–acanthocephalan relationship? A case study in a biological invasion context

8 pages; International audience; Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan…

Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression?

Manipulative endoparasites can alter the behaviour and the physiology of their intermediate hosts in ways that increase the probability of successful transmission to the final host. This requires that the parasite is able to circumvent its host's immune defence. Successful immune evasion may depend on host-parasite coevolutionary history and the appearance of new hosts invading the local host population may promote local parasite maladaptation. To test this hypothesis, we examined the effect of 2 acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on the immunity of their local and new invasive gammarid intermediate hosts, respectively Gammarus pulex and Gammarus roese…

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation.

10 pages; International audience; Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources o…

High food quality increases infection of Gammarus pulex (Crustacea: Amphipoda) by the acanthocephalan parasite Pomphorhynchus laevis.

13 pages; International audience; Parasitism is an important process in ecosystems, but has been largely neglected in ecosystem research. However, parasites are involved in most trophic links in food webs with, in turn, a major role in community structure and ecosystem processes. Several studies have shown that higher nutrient availability in ecosystems tends to increase the prevalence of parasites. Yet, most of these studies focused on resource availability, whereas studies investigating resource quality remain scarce. In this study, we tested the impact of the quality of host food resources on infection by parasites, as well as on the consequences for the host. Three resources were used t…

Sperm depletion, male mating behaviour and reproductive ‘time-out' in Gammarus pulex (Crustacea, Amphipoda).

6 pages; International audience; In Gammarus pulex, male–male competition is generally intense because the operational sex ratio (OSR) is strongly biased towards males; however, studies have shown possible fluctuation in this intrasexual competition, which could be caused by sperm depletion, a phenomenon recently found in gammarids. Sperm depletion may also affect male mating behaviour. We therefore tested the influence of sperm depletion on the OSR in G. pulex. Two sets of experiments were conducted: first, to find out the number of sperm in the testis before and after mating events (sperm depletion), and second, to test the implications of sperm depletion for the mating behaviour of male …

Evidence for a new feminizing Wolbachia strain in the isopod Armadillidium vulgare: evolutionary implications.

Wolbachia are intracellular maternally inherited alpha-Proteobacteria infecting a wide range of arthropods. In the common pill bug Armadillidium vulgare, the known Wolbachia strain is responsible for feminization of genetic males. We have investigated Wolbachia diversity in 20 populations of A. vulgare from west and east Europe, north Africa and north America. A new Wolbachia strain (wVulM) was identified through the variability of the wsp gene, distantly related to that previously known (wVulC) in this host species. No individual with multiple infections was detected. Inoculation experiments indicated that the new wVulM bacterial strain also induces feminization in A. vulgare. However, the…

Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR.

8 pages; International audience; Haemosporidian parasites are common in birds in which they act as an important selective pressure. While most studies so far have focused on the effect of their prevalence on host life-history traits, no study has measured the effect of parasitaemia. We developed molecular methods to detect, identify and quantify haemosporidia in 2 natural populations of the Blackbird Turdus merula. Three different parasite genotypes were found - 1 Haemoproteus and 2 Plasmodium. A PCR-RFLP screening revealed that only approximately 3% of blackbirds were free of parasites, compared to the 34% of uninfected birds estimated by blood smear screening. A quantitative PCR (q-PCR) a…

Additive effects of temperature and infection with an acanthocephalan parasite on the shredding activity of Gammarus fossarum (Crustacea: Amphipoda): the importance of aggregative behavior.

10 pages; International audience; Climate change can have critical impacts on the ecological role of keystone species, leading to subsequent alterations within ecosystems. The consequences of climate change may be best predicted by understanding its interaction with the cumulative effects of other stressors, although this approach is rarely adopted. However, whether this interaction is additive or interactive can hardly be predicted from studies examining a single factor at a time. In particular, biotic interactions are known to induce modifications in the functional role of many species. Here, we explored the effect of temperature on leaf consumption by a keystone freshwater shredder, the …

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

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…

Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex

SUMMARYSome parasites with complex life-cycles are able to manipulate the behaviour of their intermediate hosts in a way that increases their transmission to the next host. Gammarids infected by the tapeworm Cyathocephalus truncatus (Cestoda: Spathebothriidea) are known to be more predated by fish than uninfected ones, but potential behavioural manipulation by the parasite has never been investigated. In this study, we tested the hypothesis that C. truncatus is able to manipulate the behaviour of one of its intermediate hosts, Gammarus pulex (Crustacea: Amphipoda). To assess if any behavioural change was linked to other phenotypic alterations, we also measured the immunity of infected and u…

Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans

16 pages; International audience; Carotenoids are diverse lipophilic natural pigments which are stored in variable amounts by animals. Given the multiple biological functions of carotenoids, such variation may have strong implications in evolutionary biology. Crustaceans such as Gammarus amphipods store large amounts of these pigments and inter-population variation occurs. While differences in parasite selective pressure have been proposed to explain this variation, the contribution of other factors such as genetic differences in the gammarid ability to assimilate and/or store pigments, and the environmental availability of carotenoids cannot be dismissed. This study investigates the relati…

Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans

Carotenoids are diverse lipophilic natural pigments which are stored in variable amounts by animals. Given the multiple biological functions of carotenoids, such variation may have strong implications in evolutionary biology. Crustaceans such as Gammarus amphipods store large amounts of these pigments and inter-population variation occurs. While differences in parasite selective pressure have been proposed to explain this variation, the contribution of other factors such as genetic differences in the gammarid ability to assimilate and/or store pigments, and the environmental availability of carotenoids cannot be dismissed. This study investigates the relative contributions of the gammarid g…

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

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…