Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala.

Although interest in Acanthocephala seems to have reached only a small community of researchers worldwide, we show in this opinion article that this group of parasites is composed of excellent model organisms for studying key questions in parasite molecular biology and cytogenetics, evolutionary ecology, and ecotoxicology. Their shared ancestry with free-living rotifers makes them an ideal group to explore the origins of the parasitic lifestyle and evolutionary drivers of host shifts and environmental transitions. They also provide useful features in the quest to decipher the proximate mechanisms of parasite-induced phenotypic alterations and better understand the evolution of behavioral manipulation. From an applied perspective, acanthocephalans' ability to accumulate contaminants offers useful opportunities to monitor the impacts - and evaluate the possible mitigation - of anthropogenic pollutants on aquatic fauna and develop the environmental parasitology framework. However, exploring these exciting research avenues will require connecting fragmentary knowledge by enlarging the taxonomic coverage of molecular and phenotypic data. In this opinion paper, we highlight the needs and opportunities of research on Acanthocephala in three main directions: (i) integrative taxonomy (including non-molecular tools) and phylogeny-based comparative analysis; (ii) ecology and evolution of life cycles, transmission strategies and host ranges; and (iii) environmental issues related to global changes, including ecotoxicology. In each section, the most promising ideas and developments are presented based on selected case studies, with the goal that the present and future generations of parasitologists further explore and increase knowledge of Acanthocephala.

Title: Accrocher la communauté scientifique à des vers à la tête pleine d'épines : faits intéressants et passionnants, lacunes dans les connaissances et perspectives pour des orientations de recherche sur les Acanthocéphales. Abstract: Bien que l'intérêt pour les acanthocéphales semble n'avoir atteint qu'un petit nombre de chercheurs dans le monde, nous montrons dans cet article que ce groupe de parasites est composé d'excellents organismes modèles pour étudier les questions en suspens en biologie moléculaire et cytogénétique, écologie évolutive et écotoxicologie. Leur ascendance partagée avec les rotifères en fait un groupe idéal pour explorer les origines du mode de vie parasitaire et les moteurs évolutifs des changements d'hôtes et des transitions environnementales. Ils présentent également des caractéristiques intéressantes pour l'étude des mécanismes proximaux sous-tendant les altérations phénotypiques induites par les parasites, et ainsi mieux comprendre l'évolution de la manipulation comportementale. D'un point de vue appliqué, la capacité des acanthocéphales à accumuler les contaminants offre des opportunités utiles pour surveiller les impacts - et évaluer les possibilités d'atténuation - des pollutions anthropiques sur la faune aquatique et développer le domaine de la parasitologie environnementale. Cependant, l'exploration de ces pistes de recherche passionnantes nécessitera de relier des connaissances fragmentaires en élargissant la couverture taxonomique des données moléculaires et phénotypiques. Dans cet article, nous présentons l'état actuel de la recherche sur les acanthocéphales selon trois axes principaux : (i) la taxonomie intégrative (y compris les outils non-moléculaires) et la phylogénie à des fins d'analyse comparative ; (ii) l'écologie et l'évolution des cycles de vie, des stratégies d'exploitation des hôtes et de transmission ; (iii) les questions environnementales liées aux changements globaux, y compris l'écotoxicologie. Dans chaque section, nous soulignons les besoins et les opportunités, en espérant que cela incitera une nouvelle génération de parasitologues à s'intéresser aux acanthocéphales.

Infection with an acanthocephalan helminth reduces anxiety-like behaviour in crustacean host.

Trophically transmitted heteroxenous parasites of diverse clades can decrease or reverse antipredator behaviours in their intermediate hosts, thereby increasing their chances of reaching their final hosts. Such behavioural alterations could result from compromised cognitive abilities affecting fear- or more generally stress-related neurophysiological pathways. We tested this hypothesis in a key model system in the study of parasitic manipulation, the fish acanthocephalan parasite Pomphorhynchus tereticollis and its intermediate crustacean host Gammarus fossarum, using the 'threat of electric shock' paradigm. We exposed uninfected and infected G. fossarum to chronic and/or acute electric shock programs at two different intensities (voltage), and then quantified their sheltering behaviour as a proxy for anxiety-like state. Infected gammarids did not express anxiety-like response to electric shocks, while uninfected gammarids hid more when exposed to acute treatments, and when exposed to the high intensity chronic treatment. Interestingly, the lack of response in infected gammarids depended on parasite developmental stage. Our results support the hypothesis that this acanthocephalan parasite impacts the general anxiety-like circuitry of their intermediate host. Further studies are needed to investigate whether it involves inappropriate processing of information, impaired integration, or altered activation of downstream pathways initiating behavioural action.

Experiment in semi-natural conditions did not confirm the influence of malaria infection on bird attractiveness to mosquitoes.

BACKGROUND: Changes in host phenotype following parasite infection are often considered as host manipulation when they seem advantageous for the parasite. However, putative cases of host manipulation by parasites are rarely tested in field-realistic conditions. Infection-induced phenotypic change cannot be conclusively considered as host manipulation if no evidence shows that this trait is adaptive for the parasite in the wild. Plasmodium sp., the parasites causing malaria in vertebrates, are hypothesized to "manipulate" their host by making their odour more attractive to mosquitoes, their vector and final host. While this is fairly well supported by studies on mice and humans, studies focusing on avian malaria give contradictory results. METHODS: In the present study, genotyped birds at different stages (uninfected, acute and chronic) of Plasmodium relictum infection were exposed, in a large outdoor aviary, to their natural vector, the mosquito Culex pipiens. RESULTS: After genotyping the blood meals of more than 650 mosquitoes, we found that mosquitoes did not bite infected birds more than they bit them before infection, nor more than they bit uninfected hosts. CONCLUSIONS: Our study highlights the importance of testing ecological behaviours under natural conditions and suggests that different processes might be at play in mammals and birds regarding potential manipulation of attractiveness by malaria parasites.

Determinants of haemosporidian single- and co-infection risks in western palearctic birds.

Understanding the drivers of infection risk helps us to detect the most at-risk species in a community and identify species whose intrinsic characteristics could act as potential reservoirs of pathogens. This knowledge is crucial if we are to predict the emergence and evolution of infectious diseases. To date, most studies have only focused on infections caused by a single parasite, leaving out co-infections. Yet, co-infections are of paramount importance in understanding the ecology and evolution of host-parasite interactions due to the wide range of effects they can have on host fitness and on the evolutionary trajectories of parasites. Here, we used a multinomial Bayesian phylogenetic modelling framework to explore the extent to which bird ecology and phylogeny impact the probability of being infected by one genus (hereafter single infection) or by multiple genera (hereafter co-infection) of haemosporidian parasites. We show that while nesting and migration behaviours influenced both the probability of being single- and co-infected, species position along the slow-fast life-history continuum and geographic range size were only pertinent in explaining variation in co-infection risk. We also found evidence for a phylogenetic conservatism regarding both single- and co-infections, indicating that phylogenetically related bird species tend to have similar infection patterns. This phylogenetic signal was four times stronger for co-infections than for single infections, suggesting that co-infections may act as a stronger selective pressure than single infections. Overall, our study underscores the combined influence of hosts' evolutionary history and attributes in determining infection risk in avian host communities. These results also suggest that co-infection risk might be under stronger deterministic control than single infection risk, potentially paving the way toward a better understanding of the emergence and evolution of infectious diseases.

Correction: Sex-biased parasitism in vector-borne disease: Vector preference?

[This corrects the article DOI: 10.1371/journal.pone.0216360.].

Sex-biased parasitism in vector-borne disease: Vector preference?

Sex-biased infections are a recurrent observation in vertebrates. In many species, males are more parasitized than females. Two potentially complementary mechanisms are often suggested to explain this pattern: sexual differences in susceptibility mainly caused by the effect of sex hormones on immunity and differential exposure to parasites. Exposure is mostly a consequence of host behavioural traits, but vector-borne parasitic infections involve another degree of complexity due to the active role of vectors in transmission. Blood-sucking insects may make choices based on cues produced by hosts. Regarding malaria, several studies highlighted a male-biased infection by Plasmodium sp in great tits (Parus major). We hypothesize that the mosquito vector, Culex pipiens, might at least partially cause this bias by being more attracted to male birds. Intrinsic variation associated to bird sex would explain a preference of mosquitoes for males. To test this hypothesis, we provide uninfected mosquitoes with a choice between uninfected male and female nestlings. Mosquito choice is assessed by sex typing of the ingested blood. We did not observe any preference for a given sex. This result does not support our prediction of a preference of mosquitoes for male great tits during the nestling period. In conclusion, mosquitoes do not seem to have an intrinsic preference for male nestlings. However, sexually divergent traits (e.g. behaviour, odour, metabolic rate) present in adults may play a role in the attraction of mosquitoes and should be investigated.

Prevalence and diversity of haemosporidian parasites in the yellow-rumped warbler hybrid zone.

Parasites can play a role in speciation, by exerting different selection pressures on different host lineages, leading to reproductive barriers in regions of possible interbreeding. Hybrid zones therefore offer an ideal system to study the effect of parasites on speciation. Here, we study a hybrid zone in the foothills of the Rocky Mountains where two yellow-rumped warbler subspecies, Setophaga coronata coronata and S. c. auduboni, interbreed. There is partial reproductive isolation between them, but no evidence of strong assortative mating within the hybrid zone, suggesting the existence of a postzygotic selection against hybrids. Here, we test whether haemosporidian parasites might play a role in selecting against hybrids between S. c. coronata and S. c. auduboni. We screened birds from five transects across the hybrid zone for three phylogenetic groupings of avian haemosporidians Plasmodium, Haemoproteus and Leucocytozoon parasites and quantified intensity of infection. Contrary to our prediction, hybrids did not have higher haemosporidian parasite prevalence. Variation in Haemoproteus prevalence was best explained by an interaction between a birds' hybrid index and elevation, while the probability of infection with Leucocytozoon parasites was only influenced by elevation. We also found no significant difference in the diversity of haemosporidian lineages between the warbler subspecies and their hybrids. Finally, intensity of infection by Haemoproteus increased significantly with elevation, but was not significantly linked to birds' hybrid index. In conclusion, our data suggest that haemosporidian parasites do not seem to play a major role in selecting against hybrids in this system.