What is the difference between marine and limnetic-terrestrial associations of nematodes with invertebrates?

Zoo- and phyto-parasitic nematodes of the order Rhabditida and zooparasites of the subclass Dorylaimia are well known, due largely to their medical, veterinarian and agricultural significance. However, there have been many switches from a free-living to a symbiotic (including parasitism) mode of existence in the evolutionary trajectories of various nematode clades. Here, we attempt to summarize all known cases of symbioses (from commensalism to true parasitism) between marine nematodes representing nonparasitic taxa and various larger animals, ranging from protists to vertebrates. Most cases are of nematodes relating to dwelling on crustaceans (ectocommensalism) or living in the body cavity and internal organs of various invertebrates (endoparasitism or parasitoidism). Ectocommensal species may differ from their free-living relatives in their longer filiform bodies and enlarged ventral and caudal glands, which may be interpreted as adaptations for the purpose of fixation on the body surface of a motile host. Endoparasitic species are characterized by deep anatomical modification, including rudimentation of the alimentary tract and hypertrophy of reproductive organs. Unlike terrestrial and limnetic invertebrates, marine invertebrates have almost no intestinal nematode dwellers. The evolutionary trajectories of nematode dwellers of marine and nonmarine invertebrates are compared.

A morphological and molecular reinvestigation of Janickina pigmentifera (Grassi, 1881) Chatton 1953 - an amoebozoan parasite of arrow-worms (Chaetognatha).

Amoebozoan parasites of arrow-worms (Chaetognatha) were isolated from their hosts living in plankton of the Bay of Villefranche (Mediterranean Sea). Based on the light microscopic characters, the amoebae were identified as Janickina pigmentifera (Grassi, 1881) by their limax locomotive form and due to the presence of the intracellular symbiont, Perkinsela amoebae, surrounded by a layer of pigment granules. Sequences of the 18S rRNA gene of both J. pigmentifera and its symbiont were obtained for the first time. The molecular phylogenetic analyses of 18S rRNA gene placed J. pigmentifera within the genus Neoparamoeba, a taxon also characterized by the presence of a symbiont, known as Perkinsela amoebae-like organism (PLO). The 18S rRNA gene sequence of P. amoebae from J. pigmentifera grouped with the sequences of 18S rRNA genes of PLOs from Neoparamoeba branchiphila and Neoparamoeba invadens. The first photo documentation of the light microscopic features of J. pigmentifera, such as locomotive form, the morphology of the nucleus and P. amoebae have been provided. The new results support the affinity of J. pigmentifera with the family Paramoebidae suggested previously based on the presence of PLO. In contrast to Janickina, typical members of Paramoebidae (Neoparamoeba and Paramoeba) have a flattened, dactylopodial locomotive form. This discrepancy in morphology can be explained by the obligate parasitic lifestyle of Janickina.

Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.

Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

A food web including parasites for kelp forests of the Santa Barbara Channel, California.

We built a high-resolution topological food web for the kelp forests of the Santa Barbara Channel, California, USA that includes parasites and significantly improves resolution compared to previous webs. The 1,098 nodes and 21,956 links in the web describe an economically, socially, and ecologically vital system. Nodes are broken into life-stages, with 549 free-living life-stages (492 species from 21 Phyla) and 549 parasitic life-stages (450 species from 10 Phyla). Links represent three kinds of trophic interactions, with 9,352 predator-prey links, 2,733 parasite-host links and 9,871 predator-parasite links. All decisions for including nodes and links are documented, and extensive metadata in the node list allows users to filter the node list to suit their research questions. The kelp-forest food web is more species-rich than any other published food web with parasites, and it has the largest proportion of parasites. Our food web may be used to predict how kelp forests may respond to change, will advance our understanding of parasites in ecosystems, and fosters development of theory that incorporates large networks.

Phylogenomics Identifies a New Major Subgroup of Apicomplexans, Marosporida class nov., with Extreme Apicoplast Genome Reduction.

The phylum Apicomplexa consists largely of obligate animal parasites that include the causative agents of human diseases such as malaria. Apicomplexans have also emerged as models to study the evolution of nonphotosynthetic plastids, as they contain a relict chloroplast known as the apicoplast. The apicoplast offers important clues into how apicomplexan parasites evolved from free-living ancestors and can provide insights into reductive organelle evolution. Here, we sequenced the transcriptomes and apicoplast genomes of three deep-branching apicomplexans, Margolisiella islandica, Aggregata octopiana, and Merocystis kathae. Phylogenomic analyses show that these taxa, together with Rhytidocystis, form a new lineage of apicomplexans that is sister to the Coccidia and Hematozoa (the lineages including most medically significant taxa). Members of this clade retain plastid genomes and the canonical apicomplexan plastid metabolism. However, the apicoplast genomes of Margolisiella and Rhytidocystis are the most reduced of any apicoplast, are extremely GC-poor, and have even lost genes for the canonical plastidial RNA polymerase. This new lineage of apicomplexans, for which we propose the class Marosporida class nov., occupies a key intermediate position in the apicomplexan phylogeny, and adds a new complexity to the models of stepwise reductive evolution of genome structure and organelle function in these parasites.

The survival and dispersal of Taenia eggs in the environment: what are the implications for transmission? A systematic review.

Taenia spp. are responsible for a substantial health and economic burden in affected populations. Knowledge of the fate of the eggs of Taenia spp. in the environment and of other factors facilitating the transmission of eggs to intermediate hosts is important for the control/elimination of infections caused by Taenia spp. The aim of this systematic review was to summarize current knowledge of the factors influencing the survival and dispersal of Taenia spp. eggs in the environment. Publications retrieved from international databases were systematically reviewed. Of the 1465 papers initially identified, data were ultimately extracted from 93 papers. The results of this systematic review indicate that survival is favoured at moderate temperatures (0-20 °C). Humidity seems to affect the survival of Taenia spp. eggs more than temperature. Under field circumstances, Taenia spp. eggs have been found to survive for up to 1 year. Taenia spp. eggs are commonly found on vegetables (0.9-30%) and in soil and water samples (0-43%), with their presence posing a risk to the consumer. Invertebrates may act as transport hosts, transferring the infection to an intermediate host, but the importance of this route of transmission is still open to question. Wastewater treatment systems are not capable of entirely eliminating Taenia spp. eggs. Access to surface water and the use of sewage sludge as fertilizer on pastures are important risk factors for bovine cysticercosis. Although information on the survival and spread of Taenia spp. eggs is available, in general the data retrieved and reviewed in this article were old, focused on very specific geographical regions and may not be relevant for other areas or not specific for different Taenia spp. Furthermore, it is unknown whether egg survival differs according to Taenia sp. Future studies are necessary to identify sustainable methods to identify and inactivate parasite eggs in the environment and reduce their spread.

Wolbachia.

Ary Hoffman introduces Wolbachia.

Cercarial swimming performance and its potential role as a key variable of trematode transmission.

Trematode transmission in aquatic habitats from molluscan intermediate host to vertebrate or invertebrate target host is typically undertaken by a free-living stage known as cercariae. Active locomotion by cercariae is a key aspect of the transmission process with the swimming speed potentially contributing to infection success. Individual cercarial species swim at different speeds but the significance of this to infection potential has not been determined. This study, using data from the scientific literature, investigates the role of swimming speed in relation to cercarial morphology, host-searching strategies and target host species. Larger cercariae swim faster than smaller ones with tail length being the principal factor controlling locomotion rates. Different cercarial morphotypes swim at different speeds, in particular, furcocercariae, with the exception of the schistosomes, being faster swimmers than mono-tailed cercariae. Host-searching behaviour has a significant influence on swimming speeds with 'active-searching' strategies swimming slower than those adopting 'active-waiting' or 'prey mimcry' strategies. Vertebrate-infecting cercariae swim faster than those infecting invertebrates with species targeting fish demonstrating the highest locomotion rates and those targeting arthropods the slowest speeds. The adaptions of individual cercarial swimming speeds to biological variables and their interactions with the physical processes of aquatic habitats are discussed.

An encrusting kleptoparasite-host interaction from the early Cambrian.

Parasite-host systems are pervasive in nature but are extremely difficult to convincingly identify in the fossil record. Here we report quantitative evidence of parasitism in the form of a unique, enduring life association between tube-dwelling organisms encrusted to densely clustered shells of a monospecific organophosphatic brachiopod assemblage from the lower Cambrian (Stage 4) of South China. Brachiopods with encrusting tubes have decreased biomass (indicating reduced fitness) compared to individuals without tubes. The encrusting tubes orient tightly in vectors matching the laminar feeding currents of the host, suggesting kleptoparasitism. With no convincing parasite-host interactions known from the Ediacaran, this widespread sessile association reveals intimate parasite-host animal systems arose in early Cambrian benthic communities and their emergence may have played a key role in driving the evolutionary and ecological innovations associated with the Cambrian radiation.

First evidence of the presence of Anisakis simplex in Crangon crangon and Contracaecum osculatum in Gammarus sp. by in situ examination of the stomach contents of cod (Gadus morhua) from the southern Baltic Sea.

Cod (Gadus morhua), an important fish species in the Baltic Sea, is the paratenic host for many parasite species, including the zoonotic nematodes, Anisakis sp. and Contracaecum osculatum. We aimed to identify which invertebrate species (found in situ in the fish stomach) are responsible for infection of cod with zoonotic nematodes. We found that Crangon crangon and Gammarus sp., both invertebrate prey species of cod, were infected with Anisakis simplex and C. osculatum, respectively. These host-parasite systems are reported here for the first time, implicating C. crangon and Gammarus sp. as sources of infection of Baltic cod with zoonotic nematodes.

The Symbiotic Spectrum: Where Do the Gregarines Fit?

Gregarine apicomplexans are closely related to parasites such as Plasmodium, Toxoplasma, and Cryptosporidium, which are causing severe health and economic burdens. Colonizing only invertebrates and having no obvious medical relevance, they are mostly ignored in 'omics' studies, although gregarines are the most basal apicomplexans and therefore key players in the understanding of the evolution of parasitism in the Apicomplexa from free-living ancestors. They belong to the largest exclusively parasitic phylum, but is this perception actually true? The effects of gregarines on their hosts seem to cover the whole spectrum of symbiosis from mutualistic to parasitic. We suggest future research directions to understand the evolutionary role of gregarines, by elucidating their biology and interaction with their hosts and the hosts' microbiota.

Endoparasites observed within invertebrates used as live food items for captive wild birds: Overview and potential risks.

To monitor and evaluate potential risks to birds' health, invertebrate species that have been used as live food items had their body contents searched for endoparasites. The contents of approximately 10,000 invertebrates were analyzed. A principal component analysis was performed to study the relationship between the presence/absence of endoparasites and the characteristics of the invertebrates. In most of them, including the species preferred by birds such as caterpillars, waxworms, mealworms, most grasshoppers, and spiders, no organism was identified. Such findings suggest a low potential for parasite transmission associated with its consumption by birds. Although they had unknown or even unlikely implications for the birds' health, gregarines, oxyurides Leidynema sp., and digenetic trematodes Monolecithotrema sp. were found in samples from woodlice, cockroaches, and centipedes, respectively. The only avian parasites observed in this study were Heterakis gallinarum in samples from earthworms and Acuaria spiralis from woodlice. Suggestively, soil invertebrates showed a higher prevalence of endoparasites and may represent a higher potential risk in comparison to the other categories of invertebrates sampled herein. Detritivory and collected origin were also explanatory variables related to the presence of endoparasites in the current study.

A New Species of Orthonectida That Parasitizes Xenoturbella bocki: Implications for Studies on Xenoturbella.

Orthonectida is a phylum of marine invertebrates known to parasitize many invertebrate animals. Because of its simple body plan, it was suggested that it belong to Mesozoa, together with Dicyemida, and that it represent the evolutionary step between unicellular organisms and multicellular animals. Recent studies, including analyses of its genomes, have clarified its phylogenetic position as a member of the Protostomia, but details such as the species diversity within the phylum and how it infects the host remain unknown. Here we report orthonectids discovered from the marine worm Xenoturbella bocki. Orthonectids were found from sections of four xenoturbellid specimens, collected eight years apart. Live females were also discovered on three separate occasions. These recurring instances of orthonectids found from Xenoturbella show that they are parasitic to the animal and not just chance contaminations. Based on morphological characters such as the presence of sexual dimorphism, the arrangement of oocytes within the female body, and the presence of crystalline inclusions in the male epidermal cells, we regard this orthonectid as a new species, Rhopalura xenoturbellae sp. nov. Since orthonectids are present within the xenoturbellid adult body, caution is needed when interpreting morphological, molecular, and experimental data from X. bocki. Further studies on R. xenoturbellae will yield important information on the fundamental biological details of orthonectids that remain unknown.

Parasites and Host Species Barriers in Animal Hybrid Zones.

Species barriers are tested in hybrid zones when gene flow occurs between hybridizing species. Hybridization can erode species barriers, lead to the introgression of adaptive traits, or remain stable through time. Outcomes in hybrid zones are influenced by divergence between the hybridizing taxa, behavior, ecology, and geography. Parasites and pathogens play a major role in host fitness and appear to have varied impacts on species barriers in hybrid zones. We comprehensively reviewed the literature on parasitism in animal hybrid zones and present an evolutionary framework within which to consider parasite-hybrid interactions. Parasites most frequently show potential to contribute to species barrier breakdown in hybrid zones, but also frequently show potential to facilitate the maintenance of species barriers. Incorporating eco-immunology, parasite community theory, and spatiotemporal approaches will be important as genomic tools allow researchers to examine parasites and hybrid zones at greater resolution and in a diversity of natural habitats.

Changes in parasite-chaetognath species assemblages in the Mexican Central Pacific before and during El Niño 1997-1998.

We investigated the seasonal and interannual changes in diversity, abundance, and prevalence of chaetognaths and their parasites collected monthly during 1996-1998 in the Mexican Central Pacific. We tested the hypothesis of a positive relationship between abundance and species richness of chaetognaths and their parasites, and investigated the influence of the 1997-1998 El Niño event on this host-parasite interaction. Of the 9 chaetognath species collected in the present study, only 7 were found to be parasitized. Of 78154 chaetognath specimens collected, 790 were parasitized (1% prevalence) with at least 1 type of epibiont (cysts, perhaps protists) and 6 types of endoparasites: protists (apicomplexans, dinoflagellates, and ciliates), digeneans, cestodes, acanthocephalans, nematodes, and other unidentified endoparasites. Cysts, digeneans, and cestodes were the most abundant parasites. Mean intensity ranged from 1-4 endoparasites and from 1-21 epibionts host-1. Zonosagitta bedoti and Flaccisagitta enflata were the most abundant chaetognath species and had the highest parasite diversity. Mesosagitta minima and Parasagitta euneritica had the highest parasite prevalence (>2%). A 2-way cluster analysis defined sampling month groups as before, during, and after the 1997-1998 El Niño. The highest abundances of chaetognaths and parasites were associated with a high thermal stratification index, salinity, and mixed layer depth. We conclude that there is a positive, non-linear correlation between the abundance of chaetognaths and their parasites. Although El Niño decreased the abundance and diversity of chaetognaths throughout the time series, the abundance and diversity of their parasites were not significantly different among hydro-climatic periods, suggesting that host abundance must decrease orders of magnitude to influence host availability for parasites.

Parasite avoidance behaviours in aquatic environments.

Parasites, including macroparasites, protists, fungi, bacteria and viruses, can impose a heavy burden upon host animals. However, hosts are not without defences. One aspect of host defence, behavioural avoidance, has been studied in the terrestrial realm for over 50 years, but was first reported from the aquatic environment approximately 20 years ago. Evidence has mounted on the importance of parasite avoidance behaviours and it is increasingly apparent that there are core similarities in the function and benefit of this defence mechanism between terrestrial and aquatic systems. However, there are also stark differences driven by the unique biotic and abiotic characteristics of terrestrial and aquatic (marine and freshwater) environments. Here, we review avoidance behaviours in a comparative framework and highlight the characteristics of each environment that drive differences in the suite of mechanisms and cues that animals use to avoid parasites. We then explore trade-offs, potential negative effects of avoidance behaviour and the influence of human activities on avoidance behaviours. We conclude that avoidance behaviours are understudied in aquatic environments but can have significant implications for disease ecology and epidemiology, especially considering the accelerating emergence and re-emergence of parasites.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Evolution of pathogen and parasite avoidance behaviours.

All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word 'disgust' to describe parasite avoidance systems, in the same way that 'fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.