The horizontal transfer (HT) of genetic material between non-mating species, common in bacteria, is increasingly being recognized as a significant force in eukaryotic evolution. Most instances of HT described so far in metazoans involve mobile genetic elements — mainly transposons — but the mechanisms enabling this exchange between widely divergent species are unknown. Gilbert et al. now show that transposable elements spread between disparate species by hitch-hiking in the genomes of parasites shared by these species. Specifically, Rhodnius prolixus, an insect that feeds on the blood of tetrapods and which is the vector of Chagas disease in humans, carries four distinct transposon families in its genome that can invade the genomes of a range of tetrapods including the opossum and squirrel monkey. One of these transposon families is also present in the pond snail Lymnaea stagnalis, a vector of trematodes infecting many vertebrates. 'Horizontal gene transfer' refers to the passage of genetic material between non-mating species. Transposable elements (transposons) may be especially prone to horizontal gene transfer, but the mechanisms by which they can spread across diverged species have been elusive. Here it is shown that transposons can spread by hitchhiking in the genomes of parasites. The amount of DNA that can be transferred in this way underscores the impact of horizontal gene transfer on genome evolution. Horizontal transfer (HT), or the passage of genetic material between non-mating species, is increasingly recognized as an important force in the evolution of eukaryotic genomes1,2. Transposons, with their inherent ability to mobilize and amplify within genomes, may be especially prone to HT3,4,5,6,7. However, the means by which transposons can spread across widely diverged species remain elusive. Here we present evidence that host–parasite interactions have promoted the HT of four transposon families between invertebrates and vertebrates. We found that Rhodnius prolixus, a triatomine bug feeding on the blood of various tetrapods and vector of Chagas’ disease in humans, carries in its genome four distinct transposon families that also invaded the genomes of a diverse, but overlapping, set of tetrapods. The bug transposons are ∼98% identical and cluster phylogenetically with those of the opossum and squirrel monkey, two of its preferred mammalian hosts in South America. We also identified one of these transposon families in the pond snail Lymnaea stagnalis, a cosmopolitan vector of trematodes infecting diverse vertebrates, whose ancestral sequence is nearly identical and clusters with those found in Old World mammals. Together these data provide evidence for a previously hypothesized role of host–parasite interactions in facilitating HT among animals3,7. Furthermore, the large amount of DNA generated by the amplification of the horizontally transferred transposons supports the idea that the exchange of genetic material between hosts and parasites influences their genomic evolution.

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A role for host–parasite interactions in the horizontal transfer of transposons across phyla

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail’s lifetime this summed up to a mass equivalent of or even exceeding the snail’s own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmer's itch) due to the high number of cercariae emitted from infected snails.

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The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis.

Background
Analysis of the data available from traditional faunistic approaches to mollusc-trematode systems covering large spatial and/or temporal scales in Europe convinced us that a parasite community approach in well-defined aquatic ecosystems is essential for the substantial advancement of our understanding of the parasite response to anthropogenic pressures in urbanised areas which are typical on a European scale. Here we describe communities of larval trematodes in two lymnaeid species, Radix auricularia and Lymnaea stagnalis in four man-made interconnected reservoirs of the Ruhr River (Germany) focusing on among- and within-reservoir variations in parasite prevalence and component community composition and structure.

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Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River.

Research on the infection of snails by trematodes has been conducted in Europe for over a hundred years. The initial poor knowledge of the intra-molluscan stages of these parasites together with the difficulty of classifying them constituted a serious obstacle to the undertaking of integrated parasitological and malacological efforts to gain a better understanding of the phenomenon. The compilation of morphological and anatomical results of research on trematode larvae resulted in the publication of keys to designate species of parasites, but was not sufficient to encourage malacologists to collaborate with parasitologists. This paper undertakes to collect data published over the last hundred years on the natural infection of European populations of freshwater snails by trematode larvae. The aim of this undertaking is to make researchers of malacofauna and, above all, experts on freshwater snails aware of the scale of the problem of molluscs being exploited as intermediate hosts of trematodes and, consequently, to encourage parasitologists and malacologists to collaborate on this phenomenon that is crucial for both parasites and hosts.

One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe

Larval stages of Plagiorchis spp. are both ubiquitous and ecologically important parasites in snail populations of freshwater ecosystems in Europe. However, difficulties in distinguishing the morphologically similar cercariae used for species identification, may lead to underestimation of species diversity. In this study, 38 isolates of Plagiorchis spp. infecting two lymnaeid snails, Lymnaea
 stagnalis (L.) and Radix auricularia (L.), in five central European freshwater ecosystems were subjected to morphological and molecular assessment. Five morphologically homogeneous and genetically distinct lineages of Plagiorchis spp. were identified via matching molecular data for the mitochondrial cytochrome c oxidase subunit I (cox1) gene with detailed morphological and morphometric data of the cercariae. Comparative sequence analysis using partial 28S rDNA and ITS1-5.8S-ITS2 sequences revealed that three distinct cox1 lineages are conspecific with Plagiorchis elegans (Rudolphi, 1802), P. maculosus (Rudolphi, 1802) and P. koreanus Ogata, 1938, respectively, whereas the lineage identified based on cercarial morphology as P. neomidis Brendow, 1970 plus a single isolate that could not be assigned to a described species, did not match any of the available sequences for Plagiorchis spp. A key to the cercariae of Plagiorchis spp. parasitising lymnaeid populations in central Europe is provided to facilitate identification.

Species diversity of Plagiorchis Lühe, 1899 (Digenea: Plagiorchiidae) in lymnaeid snails from freshwater ecosystems in central Europe revealed by molecules and morphology.

The low number of articles on naturally trematode-infected snails results from the difficulty to obtain the quantitatively representative material The main aim of our study was to check which age (size) groups of snails are the most susceptible to trematode invasion Furthermore, we examined in which season the parasite prevalence is the highest We collected Lymnaea stagnalis individuals in a nearshore zone of the Jeziorak Lake (the longest Polish lake located in northern Poland) The shell height of the snails was measured and the infestation by trematode larvae was determined The logistic regression has shown that parasite prevalence increased significantly with the snail size (with the individuals >30 mm being the most infected), the distance from the beginning of the year (ie, month) and the vicinity of summer

Jarosław Kąklewski

Papers

Infestation of Lymnaea stagnalis by digenean flukes in the Jeziorak Lake.