A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of <Emphasis Type="Italic">Microcotyle sebastis</Emphasis> (Monogenea: Platyhelminthes)

Background  

The parasitic Platyhelminthes (Neodermata) contains three parasitic groups of flatworms, each having a unique morphology, and life style: Monogenea (primarily ectoparasitic), Trematoda (endoparasitic flukes), and Cestoda (endoparasitic tapeworms). The evolutionary origin of complex life cyles (multiple obligate hosts, as found in Trematoda and Cestoda) and of endo-/ecto-parasitism in these groups is still under debate and these questions can be resolved, only if the phylogenetic position of the Monogenea within the Neodermata clade is correctly estimated.     

Homoplasy or plesiomorphy? Reconstruction of the evolutionary history of mitochondrial gene order rearrangements in the subphylum Neodermata

Recent mitogenomic studies have exposed a gene order (GO) shared by two classes, four orders and 31 species (‘common GO’) within the flatworm subphylum Neodermata. There are two possible hypotheses for this phenomenon: convergent evolution (homoplasy) or shared ancestry (plesiomorphy). To test those, we conducted a meta-analysis on all available mitogenomes to infer the evolutionary history of GO in Neodermata. To improve the resolution, we added a newly sequenced mitogenome that exhibited the common GO, Euryhaliotrema johni (Ancyrocephalinae), to the dataset. Phylogenetic analyses conducted on two datasets (nucleotides of all 36 genes and amino acid sequences of 12 protein coding genes) and four algorithms (MrBayes, RAxML, IQ-TREE and PhyloBayes) produced topology instability towards the tips, so ancestral GO reconstructions were conducted using TreeREx and MLGO programs using all eight obtained topologies, plus three unique topologies from previous studies. The results consistently supported the second hypothesis, resolving the common GO as a plesiomorphic ancestral GO for Neodermata, Cestoda, Monopisthocotylea, Cestoda + Trematoda and Cestoda + Trematoda + Monopisthocotylea. This allowed us to trace the evolutionary GO scenarios from each common ancestor to its descendants amongst the Monogenea and Cestoda classes, and propose that the common GO was most likely retained throughout all of the common ancestors, leading to the extant species possessing the common GO. Neodermatan phylogeny inferred from GOs was largely incongruent with all 11 topologies described above, but it did support the mitogenomic dataset in resolving Polyopisthocotylea as the earliest neodermatan branch. Although highly derived GOs might be of some use in resolving isolated taxonomic and phylogenetic uncertainties, we conclude that, due to the discontinuous nature of their evolution, they tend to produce artefactual phylogenetic relationships, which makes them unsuitable for phylogenetic reconstruction in Neodermata. Wider and denser sampling of neodermatan mitogenomic sequences will be needed to infer the evolutionary pathways leading to the observed diversity of GOs with confidence.     

The origins of parasitism in the platyhelminthes

Symbiotic associations have arisen independently in several groups of the largely free-living turbellarians. Morphological adaptations of turbellarians to a symbiotic way of life include suckers and adhesive glands for attachment, elaborate systems of microvilli and other epidermal structures for absorption of food, glands for the formation of cysts, cocoons and cement material, and lack of a pharynx and intestine in some species. However, many species closely resemble their free-living relatives. Egg production is greatly increased at least in some species, and life cycles are always direct. Food of symbiotic turbellarians consists of host food and/or host tissue. Ectosymbiotes show fewer physiological adaptations than entosymbiotes. The major groups of parasitic Platyhehninthes (Trematoda Aspidogastrea, Trematoda Digenea, Monogenea, Udonellidea, Cestoda including Gyrocotylidea, Amphilinidea and Eucestoda), form one monophylum, the Neodermata, characterized by a neodermis (tegument) replacing the larval epidermis, epidermal cilia with a single horizontal rootlet, sensory receptors with electron-dense collars, spermatozoa with axonemes incorporated in the sperm body by proximodistal fusion, and protonephridial flame bulbs formed by two cells each contributing a row of longitudinal ribs to the filtration apparatus. The sister group of the Neodermata is unknown but is likely to be a large taxon including the Proseriata and some other turbellarian groups. Among the Neodennata, the Aspidogastrea is likely to be the most archaic group, as indicated by DNA studies, morphology, life cycles and physiology. Aspidogastreans can survive for many days or even weeks outside a host in simple media, they show little host specificity, and have an astonishingly complex nervous system and many types of sensory receptors, both in the larva and the adult. It is suggested that Aspidogastrea were originally parasites of mlluscs (and possibly arthropods and other invertebrates) and that they are archaic forms which have remained at a stage where vertebrates represent facultative hosts or obligatory final hosts into which only the very last stages of the life cycle (maturation of the gonads) have been transferred. The complex life cycles of Digenea have evolved from the simple aspidogastrean ones by intercalation of multiplicative larval stages (sporocysts, rediae) in the mollusc host, and of cercarial stages ensuring dispersal to the now obligatory final host. Monogenea may have lost the molluscan host or evolved before the early neodermatans had acquired it. Cestoda either replaced the original molluscan with an arthropod host, retained an original arthropod host or evolved from an early neodermatan before molluscan hosts had been acquired, newly acquiring an arthropod host. Horizontal gene transfer and implications for mosaic evolution in the Platyhehninthes are discussed.     

Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms

Relationships between the three classes of Neodermata (parasitic Platyhelminthes) are much debated and restrict our understanding of the evolution of parasitism and contingent adaptations. The historic view of a sister relationship between Cestoda and Monogenea (Cercomeromorphae; larvae bearing posterior hooks) has been dismissed and the weight of evidence against monogenean monophyly has mounted. We present the nucleotide sequence of the complete mitochondrial (mt) genome of Benedenia seriolae (Monogenea: Monopisthocotylea: Capsalidae), the first complete non-gyrodactylid monopisthocotylean mt genome to be reported. We also include nucleotide sequence data for some mt protein coding genes for a second capsalid, Neobenedenia sp. Analyses of the new mt genomes with all available platyhelminth mt genomes provide new phylogenetic hypotheses, which strongly influence perspectives on the evolution of diet in the Neodermata. Our analyses do not support monogenean monophyly but confirm that the Digenea and Cestoda are each monophyletic and sister groups. Epithelial feeding monopisthocotyleans on fish hosts are basal in the Neodermata and represent the first shift to parasitism from free-living ancestors. The next evolutionary step in parasitism was a dietary change from epithelium to blood. The common ancestor of Digenea + Cestoda was monogenean-like and most likely sanguinivorous. From this ancestral condition, adult digeneans and cestodes independently evolved dietary specialisations to suit their diverse microhabitats in their final vertebrate hosts. These improved perspectives on relationships fundamentally enhance our understanding of the evolution of parasitism in the Neodermata and in particular, the evolution of diet.     

Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory

We combined nearly complete sequences of large (LSU) and small (SSU) subunit rDNA from 32 flatworm species to estimate the phylogeny of the Platyhelminthes using maximum parsimony, maximum likelihood and Bayesian inference methods. Rooted against the Catenulida, combined evidence trees offered no support for the Revertospermata, which was also rejected by constraint analysis. Generally, nodal support was higher for groupings estimated from the combined data partitions and all methods of analysis provided congruent estimates of phylogeny. The Monogenea and Proseriata were resolved as monophyletic, rejecting previous suggestions of paraphyly based on SSU and partial LSU data sets and thus supporting widely accepted morphological synapomorphies. Monophyly of the Neodermata was supported and its sister group was a clade of neoophoran 'turbellarians' to the exclusion of the Proseriata which in turn was more basal. Taxa with similar spermatology to the Neodermata ( Ichthyophaga , Notentera , Urastoma and Kronborgia ) were the sister group to Tricladida + Prolecithophora, which in turn were sister to the Rhabdocoela. Polycladida + Macrostomida + Lecithoepitheliata was the earliest divergent offshoot of the Rhabditophora. Among the Neodermata, the Cercomeromorphae (Cestoda + Monogenea) was not supported, whereas Cestoda + Trematoda was well supported. Although there is no known synapomorphy for this latter grouping, our data highlight problems associated with the 'cercomer theory' and we reject putative homologies regarding neodermatan 'cercomers' that have been sustained in the literature without careful scrutiny.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 155–171.     

Hox genes from the Polystomatidae (Platyhelminthes, Monogenea)

Hox genes form a multigenic family that play a fundamental role during the early stages of development. They are organised in a single cluster and share a 60 amino acid conserved sequence that corresponds to the DNA binding domain, i.e. the homeodomain. Sequence conservation in this region has allowed investigators to explore Hox diversity in the metazoan lineages. Within parasitic flatworms only homeobox sequences of parasite species from the Cestoda and Digenea have been reported. In the present study we surveyed species of the Polyopisthocotylea (Monogenea) in order to clarify Hox identification and diversification processes in the neodermatan lineage. From cloning of degenerative PCR products of the central region of the homeobox, we report one ParaHox and 25 new Hox sequences from 10 species of the Polystomatidae and one species of the Diclidophoridae, which extend Hox gene diversity from 46 to 72 within Neodermata. Hox sequences from the Polyopisthocotylea were annotated and classified from sequence alignments and Bayesian inferences of 178 Hox, ParaHox and related gene families recovered from all available parasitic platyhelminths and other bilaterian taxa. Our results are discussed in the light of the recent Hox evolutionary schemes. They may provide new perspectives to study the transition from turbellarians to parasitic flatworms with complex life-cycles and outline the first steps for evolutionary developmental biological approaches within platyhelminth parasites.     

First evidence of the presence of microtriches in the Gyrocotylidea

The Gyrocotylidea, a small and enigmatic group of intestinal parasites of chimaeras, has been considered to be related either to the Monogenea, or, more frequently, to the most primitive monozoic tapeworms (Cestoda), i.e., the Amphilinidea and Caryophyllidea. The present study, based on transmission electron microscopical observations of a species of Gyrocotyle from the rabbit fish, Chimaera monstrosa, in the North Atlantic, demonstrates for the first time the presence of microtriches as surface structures of gyrocotylideans. Because microtriches are considered to be an autapomorphy of tapeworms (Cestoda), in which they differ from other Neodermata (Monogenea and Trematoda), the present data represent another source of evidence in support of a close relationship between the gyrocotylideans and the tapeworms sensu stricto (Eucestoda). Simple morphology, small size, and shape uniformity of the microtriches of Gyrocotyle sp. may indicate they represent an original (plesiomorphic) form that then evolved in more derived cestode groups into a variety of types present mainly on the scolex. The microtriches of Gyrocotyle sp. resemble those found in caryophyllidean, spathebothriidean, pseudophyllidean, and trypanorhynch cestodes, which are considered to represent the most basal groups of the Eucestoda.     

Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation?

Assuming that differences or similarities in morphology among congeneric parasite species living in the same habitat are not a random pattern, several hypotheses explaining morphological differences were tested: (i) reproductive isolation, (ii) niche restriction resulting from competition, and (iii) niche specialization. Congeneric monogenean (platyhelminth) ectoparasites parasitizing the gills of one host species were used as an ecological model. Morphometric distances of the attachment organ and morphometric distances of the copulatory organ between species pairs were calculated, Levin's niche size and Renkonen niche overlap indices were applied. Our results support the prediction that the function of niche segregation is to achieve reproductive isolation of related species in order to prevent hybridization (reinforcement of reproductive barriers). Parasite species living in the same niche differ greatly in the size of copulatory organ. Moreover, species coexistence is facilitated by an increase in morphometric distances of copulatory organ and niche centre distances. Our results also show that species living in overlapping niches have similar attachment organs, which supports the prediction that morphologically similar species have the same ecological requirements within one host and suggests small effects of interspecific competition for the evolution of morphological diversity of attachment organs. Specialist adaptations also seem to facilitate species coexistence and affect the niche distribution within host species. Parasite species that can colonize more than one host species, i.e. generalists, occupy more distant niches within host species than strictly host-specific parasites. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76, 125–135.     

Comparative study of helminth parasites of fishes from the Mogi Guassu river, collected during expeditions between 1927 and 1985

This paper concerns the parasitism of Nematoda, Trematoda, Acanthocephala and Cestoda from 1027 fishes of 45 species from Mogi Guassu river, examined in the years 1927, 1946, 1947, 1962, 1983 and 1985 as a contribution to the knowledge of the parasitological fauna in 58 years. Thirty two species of nematodes, 21 of trematodes, 3 of acanthocephalans and 2 of cestodes are reported. New hosts are presented for the nematodes Cucullanus pinnai, Spirocamallanus inopinatus and Travnema travnema, for the trematode Pararhipidocotyle jeffersoni and for the acanthocephalan Gorytocephalus spectabilis. New measurements for the trematode Creptotrema lynchy, tables, graphics and a list of the examined hosts with their parasites are presented.     

Origin and evolution of the hamuli in the monogeneans

The hypothesis of the origin and evolution of the hamuli in monogeneans is proposed. It is suggested that the hamuli originated as the adult attachment organs of protomonogeneans inhabited the gills of the first vertebrates. Primarily they were represented by two lateral pairs of large hooks disposed anterior to the larval haptor. The fundamental direction in the evolution of monogeneans was the concentration of all attachment structures on the growing haptor. It the course of this evolutionary process, the hamuli onchoblasts migrated to the haptor, in which they had reached the position in the hind part of the haptor. The neotenic evolution of the Dactylogyridea and Gyrodactyloidea resulted in the forming new hamuli pairs. The hooks of opposite sides of the haptor are joined in a single complex within each side by the transverse plates (bars). So the presence of 4 hamuli is plesiomorphy for all the monogeneans and the presence of the transverse bars and new hamuli pairs are apomorphy for the Dactylogyridea and Gyrodactyloidea, whose evolution was linked with that of the Teleostei. The origin of the new hamuli pairs and transverse bars in the Dactylogyridea and Gyrodactyloidea appears to be a convergence.     

How to catch a parasite: Parasite Niche Modeler (PaNic) meets Fishbase

Parasite Niche Modeler (PaNic) is a free online software tool that suggests potential hosts for fish parasites. For a particular parasite species from the major helminth groups (Acanthocephala, Cestoda, Monogenea, Nematoda, Trematoda), PaNic takes data from known hosts (maximum body length, growth rate, life span, age at first maturity, trophic level, phylogeny, and biogeography) and hypothesizes similar fish species that might serve as hosts to that parasite. Users can give varying weights to host attributes and create custom models. In addition to suggesting plausible hosts (with varying degrees of confidence), the models indicate known host species that appear to be outliers in comparison to other known hosts. These unique features make PaNic an innovative tool for addressing both theoretical and applied questions in fish parasitology. PaNic can be accessed at < http://purl.oclc.org/fishpest >.     

Global spread of helminth parasites at the human–domestic animal–wildlife interface

Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the strength of biotic and biogeographical factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite (Nematoda, Cestoda, Trematoda) sharing between mammalian wildlife species and domestic mammal hosts (including humans) using >24,000 unique country‐level records of host–parasite associations. We used hierarchical modelling and species trait data to determine possible drivers of the level of parasite sharing between wildlife species and either humans or domestic animal hosts. We found the diet of wildlife species to be a strong predictor of levels of helminth parasite sharing with humans and domestic animals, followed by a moderate effect of zoogeographical region and minor effects of species’ habitat and climatic niches. Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species (including humans). These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species. If the dietary profile and position in the trophic chain of a wildlife species largely drives its level of helminth parasite sharing with humans/domestic animals, future range shifts of host species that result in novel trophic interactions may likely increase parasite host shifting and have important ramifications for human and animal health.     

Helminthes of the water vole <Emphasis Type="Italic">Arvicola terrestris</Emphasis> Linnaeus of forest-bog biocenoses in the north of the Baraba Lowland

The results of helminthological studies of the wintered water voles are given. This group of voles hosts 13 species of helminthes: 1, Trematoda, 7, Cestoda, and 5, Nematoda. The trematode Notocotilus noyeri Joyex, 1922 (88 ±2.7)% and the cestode Arvicolepis transfuga (Spassky et Merkusheva, 1967) (68.9 ± 3.8)% dominate among them in the extensiveness of invasion (EI). The factors are studied that determine the probability of the water voles being infected with the background species of helminthes. A relation of the long-term dynamics of the host population with the dynamics of the infection with the dominant species of the parasites is established.     

The nature and evolution of the association among digeneans, molluscs and fishes

Patterns of association of digenean families and their mollusc and vertebrate hosts are assessed by way of a new database containing information on over 1000 species of digeneans for life-cycles and over 5000 species from fishes. Analysis of the distribution of digenean families in molluscs suggests that the group was associated primitively with gastropods and that infection of polychaetes, bivalves and scaphopods are all the results of host-switching. For the vertebrates, infections of agnathans and chondrichthyans are apparently the result of host-switching from teleosts. For digenean families the ratio of orders of fishes infected to superfamilies of molluscs infected ranges from 0.5 (Mesometridae) to 16 (Bivesiculidae) and has a mean of 5.6. Individual patterns of host association of 13 digenean families and superfamilies are reviewed. Two, Bucephalidae and Sanguinicolidae, are exceptional in infecting a range of first intermediate hosts qualitatively as broad as their range of definitive hosts. No well-studied taxon shows narrower association with vertebrate than with mollusc clades. The range of definitive hosts of digeneans is characteristically defined by eco-physiological similarity rather than phylogenetic relationship. The range of associations of digenean families with mollusc taxa is generally much narrower. These data are considered in the light of ideas about the significance of different forms of host association. If Manter's Second Rule (the longer the association with a host group, the more pronounced the specificity exhibited by the parasite group) is invoked, then the data may suggest that the Digenea first parasitised molluscs before adopting vertebrate hosts. This interpretation is consistent with most previous ideas about the evolution of the Digenea but contrary to current interpretations based on the monophyly of the Neodermata. The basis of Manter's Second Rule is, however, considered too flimsy for this interpretation to be robust. Problems of the inference of the evolution of patterns of parasitism in the Neodermata are discussed and considered so intractable that the truth may be presently unknowable.     

Evolutionary expansion of the Monogenea

The evolutionary expansion of the monogeneans has taken place in parallel with the diversification of the fish-like vertebrates. In this article the main trends in monogenean evolution are traced from a hypothetical skin-parasitic ancestor on early vertebrates. Special consideration is given to the following topics: early divergence between skin feeders and blood feeders; diversification and specialization of the haptor for attachment to skin; transfer from host to host, viviparity and the success of the gyrodactylids; predation on skin parasites and camouflage; colonization of the buccal and branchial cavities; diversification and specialization of the haptor for attachment to the gills; phoresy in gill parasites; the development of endoparasitism and the origin of the cestodes; the success of dactylogyroidean gill parasites; the uniqueness of the polyopisthocotyleans; ovoviviparity and the colonization of the tetrapods. Host specificity has been the guiding force of coevolution between monogeneans and their vertebrate hosts, but the establishment of monogeneans on unrelated hosts sharing the same environment (host-switching) may have been underestimated. Host-switching has provided significant opportunities for evolutionary change of direction and is probably responsible for the establishment of monogeneans on cephalopod molluscs, on the hippopotamus and possibly on chelonians. There are indications that host-switching may be more common in monogeneans that spread by direct transfer of adults/juveniles from host to host. A limitation on the further expansion of monogeneans is the need for water for the dispersal of the infective larva (oncomiracidium).     

Evolution of monogenean parasites across vertebrate hosts illuminated by the phylogenetic position of Euzetrema Combes, 1965 within the Monopisthocotylea

The Monogenea, which is divided into two clades, namely the Monopisthocotylea and Polyopisthocotylea, is a highly diversified group of platyhelminth parasites that infest mainly actinopterygian and chondrichthyan fishes but also, to a lesser extent, freshwater sarcopterygian hosts. Euzetrema knoepffleri Combes, 1965 (Monogenea: Iagotrematidae), which is specific to the salamander Euproctus montanus Savi, 1838 is among the rare monopisthocotylean parasites infesting tetrapod hosts. We sequenced the complete 18S rRNA gene of this parasite to infer its phylogenetic position within the Monopisthocotylea. Our results provide a new insight for coevolutionary scenarios between monopisthocotyleans and gnathostomatan hosts. Indeed, the basal position of E. knoepffleri within a subgroup of the Monopisthocotylea which comprises two clusters that both include parasites of the Actinopterygii and Chondrichthyes, suggests a very old association between the Iagotrematidae and tetrapods. Furthermore, if we take into account a recent view of Gnathostomata evolution where bony and cartilaginous fishes are regarded as a monophyletic group, it could be argued that the Iagotrematidae arose very early, during the fish–tetrapod transition, as did the Polystomatidae, the only monogenean family of the Polyopisthocotylea that infests sarcopterygian hosts.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 727–734.     

Ultrastructure of the scolex of Orygmatobothrium schmittii (Cestoda: Phyllobothriidea)

The ultrastructure of the scolex of Orygmatobothrium schmittii (Cestoda: Phyllobothriidae) was studied using histochemistry, scanning, and transmission electron microscopy. The central bothridial structure resulted in a glandulomuscular organ formed by a mass of syncytial glands and radial muscles, with glycoprotein secretions potentially adhesive. Among the sensory receptors found on the scolex, a particular type was found surrounding the glandulomuscular organ, which might be related in the regulation of the secretions. The internal structure of the microtriches revealed a diversity of configurations according to their morphotype and distribution on the scolex. Microtriches with larger caps are thought to be useful for attachment purposes. In addition, the thick bounding membranes of the attachment organs and the circular musculature in the bothridia, seem to aid to the attachment of the scolex to the mucosa of the host.