Advances and Trends in the Molecular Systematics of the Parasitic Platyhelminthes

doi:10.1016/S0065-308X(05)60003-6

Advances in Parasitology

Volume 60, 2005, Pages 165-243

https://doi.org/10.1016/S0065-308X(05)60003-6 Get rights and content

ABSTRACT

The application of molecular systematics to the parasitic Platyhelminthes (Cestoda, Digenea and Monogenea) over the last decade has advanced our understanding of their interrelationships and evolution substantially. Here we review the current state of play and the early works that led to the molecular-based hypotheses that now predominate in the field; advances in their systematics, taxonomy, classification and phylogeny, as well as trends in species circumscription, molecular targets and analytical methods are discussed for each of the three major parasitic groups. A by-product of this effort has been an ever increasing number of parasitic flatworms characterized genetically, and the useful application of these data to the diagnosis of animal and human pathogens, and to the elucidation of life histories are presented. The final section considers future directions in the field, including taxon sampling, molecular targets of choice, and the current and future utility of mitochondrial and nuclear genomics in systematic study.

Section snippets

INTRODUCTION

From new developments in systematic theory and molecular biological techniques, notably the polymerase chain reaction, emerged the field of molecular phylogenetics and its effect has had an immediate and far-reaching impact on biology. Beyond simply coming to the fore of systematic biology, the field has facilitated the integration of comparative evolutionary thought throughout the sub-disciplines of biology, and our inferences are now richer for it. With regard to the Platyhelminthes, and

MOLECULAR SYSTEMATICS OF THE CESTODA

The Cestoda comprises more than 5000 described species (Georgiev, 2003) including the aetiological agents of hydatidiosis and cysticercosis (Echinococcus and Taenia, respectively). As adults, they are enteric parasites of all classes of vertebrates and utilize arthropods as first intermediate hosts. They have been recognized since the time of ancient Greece (Grove, 1990) and their diversity has been well documented in the last century; systematic treatments include Yamaguti (1959), Schmidt

MOLECULAR SYSTEMATICS OF THE DIGENEA

Comprising ∼18 000 nominal species, the Digenea is by far the most speciose of the three main groups of parasitic Platyhelminthes, and may well be the largest group of internal metazoan parasites of animals (Cribb et al., 2001). Despite a vast literature on the group extending back well into the eighteenth century, the classification and phylogeny of the Digenea remained unstable and the interrelationships of numerous digenean taxa, at both higher and lower taxonomic levels, unclear. Thus the

MOLECULAR SYSTEMATICS OF THE MONOGENEA

The Monogenea is the smallest of the three parasitic groups, encompassing less than half the diversity of the Cestoda and roughly one tenth that of the Digenea based on the number of described genera (Caira and Littlewood, 2001), although estimates suggest they may be far more diverse than appreciated at present (Whittington, 1998). They are primarily ectoparasites of fishes and, with notable exceptions, only rarely produce significant pathological effects to their hosts. Human beings are not

BEYOND SYSTEMATICS: MOLECULAR DIAGNOSTICS

The complexity and variation of life history strategies in cestodes and digeneans remain among the most compelling and intriguing aspects of the biology of these parasites. Elucidating their life cycles was a cornerstone of the field for much of the early part of the twentieth century, by which time the basic ontogenetic and host sequences had been worked out for most major groups. Since then, new information on life cycles diminished as parasitologists turned first to experimental, and later

Taxonomic Considerations

Early molecular phylogenetic studies of the parasitic flatworms, as in other taxa, have tended to address questions from the bottom up; that is, from the basal divergences among major lineages to subsequent investigations of divergences in more restricted and recent clades. The result is that we have a phylogenetic framework, based on one or more genes, for the phylum, the Neodermata, and for each of the major neodermatan groups. While these hypotheses require further corroboration, effort is

ACKNOWLEDGMENTS

PDO was supported by the Wellcome Trust through a senior fellowship (043965/Z/95/Z) to D.T.J. Littlewood (The Natural History Museum, UK) and VVT was supported by the National Science Foundation through North Dakota EPSCoR (Grant No 0132289). We are grateful to I. Beveridge, T. Littlewood and T. Huyse for their time and suggestions.

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The evolution of endoparasitism and complex life cycles in parasitic platyhelminths
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Within flatworms, the vast majority of parasitism is innate to Neodermata, the most derived and diversified group of the phylum Platyhelminthes.¹^,² The four major lineages of Neodermata maintain various combinations of life strategies.³ They include both externally (ecto-) and internally feeding (endo-) parasites. Some lineages complete their life cycles directly by infecting a single host, whereas others succeed only through serial infections of multiple hosts of various vertebrate and invertebrate groups. Food sources and modes of digestion add further combinatorial layers to the often incompletely understood mosaic of neodermatan life histories. Their evolutionary trajectories have remained molecularly unresolved because of conflicting evolutionary inferences and a lack of genomic data.⁴ Here, we generated transcriptomes for nine early branching neodermatan representatives and performed detailed phylogenomic analyses to address these critical gaps. Polyopisthocotylea, mostly hematophagous ectoparasites, form a group with the mostly hematophagous but endoparasitic trematodes (Trematoda), rather than sharing a common ancestor with Monopisthocotylea, ectoparasitic epithelial feeders. Phylogenetic placement of the highly specialized endoparasitic Cestoda alters depending on the model. Regardless of this uncertainty, this study brings an unconventional perspective on the evolution of platyhelminth parasitism, rejecting a common origin for the endoparasitic lifestyle intrinsic to cestodes and trematodes. Instead, our data indicate that complex life cycles and invasion of vertebrates’ gut lumen, the hallmark features of these parasites, evolved independently within Neodermata. We propose the demise of the traditionally recognized class Monogenea and the promotion of its two subclasses to the class level as Monopisthocotyla new class and Polyopisthocotyla new class.
First record of Metapolystoma (Monogenea: Polystomatidae) from Boophis tree frogs in Madagascar, with the description of five new species
2021, International Journal for Parasitology: Parasites and Wildlife
Citation Excerpt :
This separation of Metapolystoma and Polystoma was based on morphological characters, including the large extended uterus containing many eggs that fills the largest part of the body and the posterior position of the large ovary (Combes, 1976). The validity of Metapolystoma as a genus has however been under dispute ever since its nested position within Polystoma was demonstrated at the molecular level (Bentz et al., 2001; Verneau et al., 2002; Olson and Tkach, 2005). Up to the present, the three known Metapolystoma species have been described from grass frogs belonging to Ptychadena: M. brygoonis from P. mascareniensis in Madagascar, M. cachani (Gallien, 1956) from Ptychadena longirostris (Peters, 1870) in Ivory Coast and Metapolystoma porosissimae du Preez and Kok 1992, from Ptychadena porosissima (Steindachner, 1867) in South Africa.
Although Madagascar has more than 350 frog species of which all but two are endemic to the island, the known polystome (Monogenea: Polystomatidae) diversity parasitizing Malagasy frogs is low, encompassing five species of Madapolystoma, one species of Kankana and one Metapolystoma. Investigating the parasite diversity of frog parasites at selected Malagasy localities led to the discovery of undescribed polystomes. Five treefrogs, Boophis albilabris, Boophis doulioti, Boophis luteus, Boophis madagascariensis and Boophis occidentalis were found to be infected and are reported here as hosts for new Metapolystoma species. Morphological investigation, combining examination of body length, haptor length, genital bulb width, genital crown diameter, genital spine number, genital spine length, ovary length, egg length, hamulus length, hamulus guard length and hamulus hook length, revealed five distinct morphotypes. Phylogenetic analysis and genetic divergences obtained for three of the five morphotypes, support the distinction of new species. Metapolystoma ansuanum n. sp. is described from B. luteus, Metapolystoma falcatum n. sp. from B. doulioti, Metapolystoma multiova n. sp. from B. occidentalis, Metapolystoma theroni n. sp. from B. madagascareniensis and Metapolystoma vencesi n. sp. from B. albilabris. Finally, although the validity of Metapolystoma as taxon is not fully resolved yet, the phylogenetic position of the described species and their morphology provide clear evidence for new metapolystome taxa.
The state of fish parasite discovery and taxonomy: a critical assessment and a look forward
2020, International Journal for Parasitology
Efforts to find and characterise new parasite species in fish hosts are crucial not just to complete our inventory of Earth’s biodiversity, but also to monitor and mitigate disease threats in fisheries and aquaculture in the face of global climate change. Here, we review recent quantitative assessments of research efforts into fish parasite discovery and taxonomy. We address broad questions including: Are efforts aimed at finding new parasite species targeted at geographical hotspots of fish biodiversity, where there should be more parasite species to be found? Is the application of molecular tools to study parasite genetic diversity deployed strategically across regions of the world, or focused disproportionately on certain areas? How well coordinated is the search for new parasite species of fish among workers specialising on different higher helminth taxa? Are parasite discovery efforts in any geographical area consistent over time, or subject to idiosyncrasies due to the waxing and waning of highly prolific research careers? Is the quality of taxonomic descriptions of new species improving over time, with the incorporation of new tools to characterise species? Are taxonomic descriptions moving away from a focus on the adult stage only toward attempts to characterise the full life cycle of newly-discovered helminth species? By using empirical evidence to answer these questions, we assess the current state of research into fish parasite discovery and taxonomy. We also explore the far-reaching implications of recent research on parasite microbiomes for parasite taxonomy. We end with recommendations aimed at maximising the knowledge gained per fish sacrificed, and per dollar and time invested into research on fish parasite biodiversity.
Morphological and molecular characterization of six Indian Tetracotyle type metacercariae (Digenea: Strigeidae Railliet, 1919), using ribosomal and mitochondrial DNA
2019, Parasitology International
Strigeids have a cup-shaped fore body, containing a holdfast organ with two lobes and hind body. The species diversity of strigeids remains incomplete, especially in the Indian sub-continent. Here, we described six Tetracotyle type metacercariae (T. muscularis, T. fausti, T. lucknowensis, T. xenentodoni, T. mathuraensis and T. glossogobii) from five fresh water fish, collected at Lucknow (India). Next, we characterized these metacercariae using ribosomal (18S, 28S, ITS2) and mitochondrial DNA (COI) to determine their systematic and phylogenetic position. Molecular identification using inter-specific variation range for all four molecular markers revealed 1.9–4.9% (18S); 3.3–8.8% (28S); 6.8–12.9% (ITS2), and 3.5–9.4% (COI) among six Tetracotyle type metacercariae. In phylogenetic analysis, constructed by neighbour-joining (NJ) and maximum likelihood (ML) methods, T. fausti, T. glossogobii, T. xenentodoni, T. lucknowensis and T. mathuraenis nested as sister groups with the member of strigeids for all four markers used; T. muscularis, however, formed a basal clade. Furthermore, phylogenetic placement states the monophyly of the Tetracotyle type of metacercariae in all the markers (18S, 28S, COI), except ITS2.
Taxonomic and geographic bias in the genetic study of helminth parasites
2019, International Journal for Parasitology
The use of genetic information is now fundamental in parasite taxonomy and systematics, for resolving parasite phylogenies, discovering cryptic species, and elucidating patterns of gene flow among parasite populations. The accumulation of available gene sequences per geographical area or per parasite taxonomic group is likely proportional to species richness, but not without some biases. Certain areas and certain taxonomic groups receive more research effort than others, possibly causing a deficit in the relative number of parasite species being characterized genetically in some areas or taxonomic groups. Here, we use data on the number of parasite records per country or helminth family from the London Natural History Museum host-parasite database, and matching data on the number of gene sequences available from the National Center for Biotechnology Information (NCBI) GenBank database, to determine how available gene sequences scale with species richness across countries or parasitic helminth families. Our quantitative analysis identified countries/regions of the world and helminth families that have received the most effort in genetic research. More importantly, it allowed us to generate lists (based on residuals from the statistical model) of the 20 countries/regions and the 20 helminth families with the largest deficit in available gene sequences relative to their helminth species richness. We propose these lists as useful guides toward future allocation of effort to maximise advances in parasite biodiscovery, systematics and population structure.
Evidence that blood flukes (Trematoda: Aporocotylidae) of chondrichthyans infect bivalves as intermediate hosts: indications of an ancient diversification of the Schistosomatoidea
2017, International Journal for Parasitology
Blood flukes (Aporocotylidae) of actinopterygians (bony fishes) have been shown to infect freshwater gastropods and marine polychaetes as intermediate hosts. However, no life cycle is known for any aporocotylid of chondrichthyans (cartilaginous fishes) and no adult aporocotylid has been linked to a cercaria infecting a bivalve. Here we report two novel infections that fill these gaps. Cercariae consistent with the family Aporocotylidae were found developing in sporocysts in the gonad of the surf pipi, Donax deltoides Lamarck, 1818 (Bivalvia: Donacidae), from Stockton Beach, central New South Wales, Australia. Adult aporocotylids were found in the heart of the giant shovelnose ray, Glaucostegus typus (Anonymous [Bennett], 1830), from Moreton Bay, southeastern Queensland, Australia. Phylogenetic analyses of the 28S rDNA region generated from the new specimens resulted in phylograms in which the two parasites form a strongly supported clade with Chimaerohemecus trondheimensis van der Land, 1967, the only aporocotylid known from a holocephalan and the only other chondrichthyan-infecting aporocotylid for which sequence data are available. Most marine aporocotylids of actinopterygians also form a strongly supported clade. These findings lead us to hypothesise that the aporocotylids of chondrichthyans are distinct from all other blood flukes in infecting bivalves as intermediate hosts. Putative cophyly between three major blood fluke clades and both definitive and intermediate host groups is consistent with diversification of the Schistosomatoidea over 400 million years ago.

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Advances and Trends in the Molecular Systematics of the Parasitic Platyhelminthes

ABSTRACT

Section snippets

INTRODUCTION

MOLECULAR SYSTEMATICS OF THE CESTODA

MOLECULAR SYSTEMATICS OF THE DIGENEA

MOLECULAR SYSTEMATICS OF THE MONOGENEA

BEYOND SYSTEMATICS: MOLECULAR DIAGNOSTICS

Taxonomic Considerations

ACKNOWLEDGMENTS

International Journal for Parasitology

Parasitology International

Systematic Parasitology

International Journal for Parasitology

Molecular and Biochemical Parasitology

International Journal for Parasitology

International Journal for Parasitology

Acta Tropica

Journal of Helminthology

Parasitology

Molecular and Biochemical Parasitology

Journal of Helminthology

Experimental Parasitology

Acta Tropica

Canadian Journal of Zoology

The Journal of Parasitology

Parasitological Research

Folia Parasitologica

Chinese Journal of Parasitology and Parasitic Diseases

Journal of Parasitology

Systematic Parasitology

Parasitology

Diseases of Aquatic Organisms

Diseases of Aquatic Organisms

Electrophoretic demonstration of polymorphism of glucosephosphate isomerase in natural populations of Paragonimus miyazakii

Journal of Parasitology

Genetic variability and differentiation of natural populations in three Japanese lung flukes, Paragonimus ohirai, Paragonimus iloktsuenensis and Paragonimus sadoensis (Digenea: Troglotrematidae)

Journal of Parasitology

Population genetic studies on isozymes in Paragonimus westermani from the Philippines

Japanese Journal of Parasitology

The origin of the triploid in Paragonimus westermani on the basis of variable regions in the mitochondrial DNA

Journal of Helminthology

Electrophoretic analysis of a natural population of the Thai Paragonimus heterotremus and its genetic relationship to the three Japanese species P. miyazakii, P. ohirai and P. westermani

Parasitology Research

Electrophoretic studies on enzymes in Paragonimus spp. 1. Comparison of isozyme patterns between P. ohirai and P. miyazakii

Japanese Journal of Parasitology

Genetic variation in the triploids of Japanese Fasciola species, and relationships with other species in the genus

Journal of Helminthology

Mitochondrial DNA differentiation of Japanese diploid and triploid Paragonimus westermanni

Journal of Helminthology

Evidence for a clade of nematodes, arthropods and other moulting animals

Nature

Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dolphins (Stenella coeruleoalba) from the Western Mediterranean

Parasitology

Identifications and maturation of the metacercaria of Indodidymozoon pearsoni (Digenea: Didymozoidae)

Journal of Helminthology

Species differentiation in the Didymozoidae (Digenea) restriction fragment length differences in internal transcribed spacer and 5.8s ribosomal DNA

International Journal for Parasitology

Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics

International Journal for Parasitology

The Parasites of Homo Sapiens. An Annotated Checklist of the Protozoa, Helminths and Arthropods for Which We are Home

Thin layer chromatographic analyses of amino acids in Echinostoma revolutum (Trematoda) adults

International Journal for Parasitology

Host specificity dynamics: observations on gyrodactylid monogeneans

International Journal for Parasitology

The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data

Journal of Parasitology

Conflicting phylogenetic hypotheses for the parasitic platyhelminths tested by partial sequencing of 18S ribosomal RNA

International Journal for Parasitology

Molecular evidence for the synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. annuligerum (von Nordmann, 1832) (Digenea: Strigeidae) parasitic as metacercariae in British fishes

Journal of Helminthology

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

Biological Journal of the Linnean Society

DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you

Trends in Parasitology