The evolutionary expansion and host-parasite relationships of the Digenea

Relevant data on the Digenea extracted from a host-parasite data-base are analysed in relation to host-groups, host-specificity, speciation, radiation and geographical distribution. The classification, evolution, co-evolution, and co-speciation of the group are discussed. Principal components analyses indicated that 119 families formed 11 groups in relation to their vertebrate hosts and the 55 families with molluscan records formed 6 groups in relation to their molluscan hosts. The most prominent host-groups are the Fish and Mammals. Individual digenean families did not exhibit the host combinations Fish + Birds, Fish + Mammals, Herpetiles + Birds and Herpetiles + Mammals. Families with Fish hosts tended to use Prosobranch and, to a lesser extent Bivalve, molluscs, whereas families in Herpetiles, Birds and Mammals tended to use Pulmonates. Families using 3 or 4 mixed vertebrate groups tended to use mixed molluscan groups. Families using Herpetiles as the vertebrate host tend to be the most host-specific and the least speciose, whereas those using 3 to 4 mixed vertebrate groups are the most speciose. In a detailed examination of three zoogonid genera, few indications of co-evolution with their vertebrate hosts were detected, and geographical information from the data-base appeared to shed no light upon the geographical origins of the Digenea. Some of these findings are commented upon in relation to the evolution of the Digenea.     

Diversity in the Monogenea and Digenea: does lifestyle matter?

If the cestodes are excluded, then the parasitic platyhelminths of fishes divide neatly into the external and monoxenous Monogenea and the internal and heteroxenous Digenea. Both groups have apparently had long associations of coevolution, host switching and adaptation with fishes and have become highly successful in their respective habitats. Current estimates of species richness for the two groups suggest that they may be remarkably similar. Here we consider the nature of the diversity of the Monogenea and Digenea of fishes in terms of richness of species and higher taxa to determine what processes may be responsible for observed differences. The Monogenea includes at least two super-genera (Dactylogyrus and Gyrodactylus) each of which has hundreds of species; no comparable genera are found in the Digenea. Possible reasons for this difference include the higher host specificity of monogeneans and their shorter generation time. If allowance is made for the vagaries of taxonomic 'lumping' and 'splitting', then there are probably comparable numbers of families of monogeneans and digeneans in fishes. However, the nature of the families differ profoundly. Richness in higher taxa (families) in the Digenea is explicable in terms of processes that appear to have been unimportant in the Monogenea. Readily identifiable sources of diversity in the Digenea are: recolonisation of fishes by taxa that arose in association with tetrapods; adoption of new sites within hosts; adoption of new diets and feeding mechanisms; adaptations relating to the exploitation of ecologically similar groups of fishes and second intermediate hosts; and adaptations relating to the exploitation of phylogenetic lineages of molluscs. In contrast, most higher- level monogenean diversity (other than that associated with the subclasses) relates principally to morphological specialisation for attachment by the haptor.     

Comparison of digenean faunas of sillaginid fishes from inshore and offshore waters of Visakhapatnam Coast, Bay of Bengal

The sillaginid fishes of Visakhapatnam Coast, Bay of Bengal, are found to be hosts for 16 species of digeneans of which seven are adult digeneans belonging to families Opecoelidae, Zoogonidae and Hemiuridae and nine are larval digeneans representing families Bucephalidae, Heterophyidae, Cryptogonimidae, Acanthocolpidae, Hemiuridae and Didymozoidae. The digenean fauna of sillaginid fishes from shallow coastal waters (< 10 m depth) and deeper offshore waters (30–50 m depth) are compared and results are discussed in the light of existing information on the migratory movements of different species of sillaginids and their occurrence in coastal or offshore waters. The usefulness of metacercariae of these fishes as 'biological tags' is considered.     

Parasitism of Molluscs by Nematodes: Types of Associations and Evolutionary Trends

Although there are no confirmed fossil records of mollusc parasitic nematodes, diverse associations of more than 108 described nematode species with slugs and snails provide a fertile ground for speculation of how mollusc parasitism evolved in nematodes. Current phylogenic resolution suggests that molluscs have been independently acquired as hosts on a number of occasions. However, molluscs are significant as hosts for only two major groups of nematodes: as intermediate hosts for metastrongyloids and as definitive hosts for a number of rhabditids. Of the 61 species of nematodes known to use molluscs as intermediate hosts, 49 belong to Metastrongyloidea (Order Strongylida); of the 47 species of nematodes that use molluscs as definitive hosts, 33 belong to the Order Rhabditida. Recent phylogenetic hypotheses have been unable to resolve whether metastrongyloids are sister taxa to those rhabditids that use molluscs as definitive hosts. Although most rhabditid nematodes have been reported not to kill their mollusc hosts prior to their reproduction, some species are pathogenic. In fact, infective juveniles of Phasmarhabditis hermaphrodita vector a lethal bacterium into the slug host in which they reproduce. This life cycle is remarkably similar to the entomopathogenic nematodes in the families Steinernematidae and Heterorhabditidae. Also, the discoveries of Alloionema and Pellioditis in slugs are interesting, as these species have been speculated to represent the ancestral forms of the entomopathogenic nematodes. Development of the infective stage appears to be an important step toward the acquisition of molluscs as definitive hosts, and the association with specific bacteria may have arisen in conjunction with the evolution of necromeny.     

Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons

Attention is drawn to the effects of parasites on their hosts, taking as a model the digenean parasites of teleosts (hereafter: fish) from lagoons along the French Mediterranean coast. Because digeneans have a heteroxenic life cycle, their impact is not limited to the definitive host, which harbours the sexual adults, but is extended to the first host (mollusc) and to the second host ("invertebrate" or fish). Adult parasites, in order to ensure efficient sexual reproduction, never cause excessive damage to their definitive host, usually only exploiting the intestinal fluids; however, the host must intensify its search for prey, which results in a diminished fitness. Within the first host, 'larval' stages of digenean parasites invade the gonads, resulting in its castration, then exhaustion and eventually death. The diversion of energy from the second hosts towards the parasites forces them to intensify their search for food, resulting in decreased fitness and an increased risk of being eaten; in addition, manipulation of the host's behaviour by parasites drives this host into the food chain of the definitive host. In lagoons, many individuals of almost all species of fish and invertebrates act as first, second and/or definitive hosts for digeneans. Obviously, parasites have a severe impact on the population dynamics of key taxa, on the food web and therefore also on the functioning of the whole lagoon ecosystem. Yet this impact has been largely overlooked or underestimated in functioning models, by ecologists, who tend to prioritize more apparent trophic relationships.     

V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data

There is no morphological synapomorphy for the disparate digeneans, the Fellodistomidae Nicoll, 1909. Although all known life-cycles of the group include bivalves as first intermediate hosts, there is no convincing morphological synapomorphy that can be used to unite the group. Sequences from the V4 region of small subunit (18S) rRNA genes were used to infer phylogenetic relationships among 13 species of Fellodistomidae from four subfamilies and eight species from seven other digenean families: Bivesiculidae; Brachylaimidae; Bucephalidae; Gorgoderidae; Gymnophallidae; Opecoelidae; and Zoogonidae. Outgroup comparison was made initially with an aspidogastrean. Various species from the other digenean families were used as outgroups in subsequent analyses. Three methods of analysis indicated polyphyly of the Fellodistomidae and at least two independent radiations of the subfamilies, such that they were more closely associated with other digeneans than to each other. The Tandanicolinae was monophyletic (100% bootstrap support) and was weakly associated with the Gymnophallidae (<50–55% bootstrap support). Monophyly of the Baccigerinae was supported with 78–87% bootstrap support, and monophyly of the Zoogonidae + Baccigerinae received 77–86% support. The remaining fellodistomid species, Fellodistomum fellis, F. agnotum and Coomera brayi (Fellodistominae) plus Proctoeces maculatus and Complexobursa sp. (Proctoecinae), formed a separate clade with 74–92% bootstrap support. On the basis of molecular, morphological and life-cycle evidence, the subfamilies Baccigerinae and Tandanicolinae are removed from the Fellodistomidae and promoted to familial status. The Baccigerinae is promoted under the senior synonym Faustulidae Poche, 1926, and the Echinobrevicecinae Dronen, Blend & McEachran, 1994 is synonymised with the Faustulidae. Consequently, species that were formerly in the Fellodistomidae are now distributed in three families: Fellodistomidae; Faustulidae (syn. Baccigerinae Yamaguti, 1954); and Tandanicolidae Johnston, 1927. We infer that the use of bivalves as intermediate hosts by this broad range of families indicates multiple host-switching events within the radiation of the Digenea.     

Ecological approach to the problem of monophyly of Neodermata (Platyhelminthes)

The ecological scenario of the evolution of main branches of Neodermata is described. The first neodermateans (= promonogeneans) were parasites of the gill lamellae of Paleozoic jawless vertebrates, which were microphagous suspension-feeding animals. The main apomorphic characters of the primary neodermateans are neodermis, cercomer (posterior hooked attachment organ) and swimming infective larva. All subsequent evolution of Neodermata was related with their acquisition new niches in hosts, which were intensively diverging in that time adapting to new food types and conquering new ecological niches. The acquisition of new microhabitats was accompanied by the development of morphological diversity in Neodermata especially in a structure of attachment and genital organs. Trematoda, Cestoda and Polyopisthocotylea comprise specialized evolutionary lineages and Monopisthocotylea is a basal taxon. Polyopisthocotylea is specialized to the blood feeding on fish gills. The common ancestors of the Trematoda and Cestoda inhabited walls of gills and pharyngeal cavities, from where they penetrated the digestive tract. The aspidogastridean multiloculate hold fast appears to be a highly specialized attachment organ of the monogenean ancestor, which inhabited muscular pharyngeal walls of Paleozoic vertebrates. The loss of cercomer hooks probably took place when mollusk-hosts have been involved in the aspidogastridean life cycle. The extinction of many chondrichthiean groups and progress of small plankton fishes (Teleostei) has led to the appearance Digenea. New vertebrate hosts needed a new infestation type and the cercaria appeared. Parthenogenesis has been developed in stages living in mollusks to counterbalance the loss of individuals at two transmission stages in the digenean cycle; this was resulted in a strong specificity to mollusk-host. Evolutionary tendencies of Trematoda and Cestoda show noticeable similarities.     

The origins and evolutionary expansion of the Strongylida (Nematoda)

The Strongylida are thought to have arisen from free-living rhabditoid nematodes, but the relationships between the major groupings within the Strongylida, the Strongylina, the Metastrongylina, Trichostrongylina and the Ancylostomatina are far from clear in spite of the abundance of morphological data now available for analysis. Evolutionary mechanisms including co-evolution, host switching, host dispersal, use of intermediate hosts, various sites of localisation within the definitive host and modifications of life-cycle strategies appear to have been utilised in the expansion of the Strongylida, with different mechanisms predominating in different families or superfamilies. Co-evolution appears to have been a major mode of evolution in the Strongylina, in contrast to the Trichostrongylina, which have used host dispersal and host-switching to great advantage. The phylogeny of the Ancylostomatina shows little association with host evolution, but does match the feeding preferences of the hosts. The Metastrongylina have utilised intermediate hosts and life cycle modifications including a shift to extra-intestinal sites as major means of diversification, in contrast to the other sub-orders. The review, while indicating much progress in our understanding of the phylogeny of the Strongylida, also reveals that enormous gaps still exist, and emphasises the tentative nature of many of the phylogenetic hypotheses tendered to date.     

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.     

Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae)

The maintenance of strict host specificity by parasites when several closely related host species live in sympatry is poorly understood. Species of intertidal trochid snails in the genera Diloma, Melagraphia and Austrocochlea often occur together and are parasitised by a single digenean morphotype (Platyhelminthes, Trematoda), tentatively placed in Opecoelidae. Of the 10 trochid species (6 from New Zealand, 4 from Australia) we examined, six were found to be infected, and the prevalence of infection was as high as 17.5%. We obtained molecular data (mitochondrial 16S and nuclear rDNA internal transcriber spacer 2 sequences, representing 774 bp), to infer phylogenetic relationships amongst these Digenea. Our phylogeny separated the single morphotype into three clearly defined clades (which are almost certainly separate biological species): (i) those infecting two species of Austrocochlea from Tasmania, (ii) those infecting Diloma subrostrata in Otago and Southland, New Zealand, and (iii) those infecting all the parasitised New Zealand topshells (Melagraphia aethiops, D. subrostrata, Diloma nigerrima and Diloma arida) throughout the country. This last group comprised two subclades, one infecting only D. subrostrata and one infecting the other three species. Two D. subrostrata populations were each found to be infected by genetically distinct parasites, yet sympatric populations of the other snails were not necessarily infected. This study is thus the first to reveal cryptic species of digeneans in a single population of a molluscan first intermediate host. We point out also that the degree of host specificity would have been grossly underestimated if, in the absence of our genetic analysis, we had only considered digenean morphology. Our results shed light on the conditions that may favour switching among intermediate hosts in digeneans, and on the presence/absence of host specificity in these parasites.     

Parasite-mediated shell alterations in Recent and Holocene sub-Antarctic bivalves: the parasite as modeler of host reaction

Abstract. New data on shell reactions elicited by larval digeneans in bivalves from Recent sub-Antarctic populations and late Holocene Patagonian deposits are reported. Shell alterations, which are traces of digenean trematode infections, were found affecting intertidal bivalve populations from Malvinas (Falkland) Islands, Burdwood Bank, Beagle Channel, and from Holocene deposits at Tierra del Fuego (Argentina). The bivalve species involved belonged to the families Nuculanidae, Cyamiidae, and Neoleptonidae. Such reactions consisted of quite unusual dome or igloo-shaped calcifications on the inner shell surface; the similarities and uniqueness of this reaction in different bivalve species reported here suggest that the invasive agent is the same. Based on previous findings of morphologically identical shell alterations in Gaimardia trapesina (Bivalvia, Gaimardiidae) from Magellanic and sub-Antarctic waters, it is suggested that the parasites responsible for the traces reported here belong to a digenean platyhelminth species of the Gymnophallidae genus Bartolius . The host bivalves reported here belong to three different superfamilies, and share a similar crystalline shell microstructure: aragonite with homogeneous structure. After a review of the available information dealing with bivalve shell-mantle reactions against digeneans, it is hypothesized that parasites are responsible for the modeling of the host response they elicit. However, although the specific characteristics of the reaction depend on the parasite, they would probably be constrained by some characteristics of the host shell structure.     

Checklist of digenean trematodes reported from Indian marine fishes

This checklist summarises information on the digenean trematodes of Indian marine fishes contained in the world literature dating from 1913 to the end of 2008. Altogether more than 700 species of digeneans belonging to more than 200 genera and 32 families are recorded. For each parasite species information is provided on the host(s), geographical locality (-ies) and the published source(s). The synonymies proposed in the literature for some of the parasite species are also included. The classification follows that given in the 'Keys to the Trematoda'.     

Digenean species diversity in teleost fishes from the Gulf of Gabes, Tunisia (Western Mediterranean)

This study is the first attempt to survey the diversity of fish digeneans in the Gulf of Gabes (southern coast of Tunisia). A total of 779 fishes belonging to 32 species were sampled. 53 species of Digenea belonging to 15 families were recorded. Among these species, 24 are reported for the first time from the coast of Tunisia. We report one new host record, Lecithochirium sp. from Sardinella aurita. The Hemiuridae is the dominant family. A host-parasite list is presented with the information on the prevalence, abundance and mean intensity of each species collected. The diversity of Digenea is compared with other localities in the Mediterranean Sea and the northern east of Tunisia. The Gulf of Gabes shows the lowest diversity linked to the anthropogenic activities and impact of exotic species. The use of Digenea as indicators of the state of the ecosystem is discussed.     

Distance decay of similarity among parasite communities of three marine invertebrate hosts

The similarity in species composition between two communities generally decays as a function of increasing distance between them. Parasite communities in vertebrate definitive hosts follow this pattern but the respective relationship in intermediate invertebrate hosts of parasites with complex life cycles is unknown. In intermediate hosts, parasite communities are affected not only by the varying vagility of their definitive hosts (dispersing infective propagules) but also by the necessary coincidence of all their hosts in environmentally suitable localities. As intermediate hosts often hardly move they do not contribute to parasite dispersal. Hence, their parasite assemblages may decrease faster in similarity with increasing distance than those in highly mobile vertebrate definitive hosts. We use published field survey data to investigate distance decay of similarity in trematode communities from three prominent coastal molluscs of the Eastern North-Atlantic: the gastropods Littorina littorea and Hydrobia ulvae, and the bivalve Cerastoderma edule. We found that the similarity of trematode communities in all three hosts decayed with distance, independently of local sampling effort, and whether or not the parasites used the mollusc as first or second intermediate host in their life cycle. In H. ulvae, the halving distance (i.e. the distance that halves the similarity from its initial similarity at 1 km distance) for the trematode species using birds as definitive hosts was approximately two to three times larger than for species using fish. The initial similarities (estimated at 1 km distance) among trematode communities were relatively higher, whereas mean halving distances were lower, compared to published values for parasite communities in vertebrate hosts. We conclude that the vagility of definitive hosts accounts for a high similarity at the local scale, while the strong decay of similarity across regions is a consequence of the low probability that all necessary hosts and suitable environmental conditions coincide on a large scale.     

Immune mechanisms in trematode-snail interactions

Digenetic trematodes, including several species of medical and veterinary significance, nearly all depend on molluscs (usually gastropods) as hosts for asexual reproduction. The molluscan internal defence system, although lacking many of the familiar features of the vertebrate immune system, may pose a substantial obstacle to digenean development. In this article, Wil van der Knaap and Eric Loker discuss the manner in which this system is mobilized to kill larval trematodes and the real and putative mechanisms of digenean evasion of molluscan immune responses. These two possible outcomes of trematode-snail associations make them intriguing model systems for exploring processes of parasite infectivity and host resistance.     

Digeneans of fishes from the Adriatic Sea with a description of Lecithaster atherinae n. sp. from Atherina (Hepsetia) boyeri

A collection of whole mount preparations of digeneans was studied. The parasites were collected from several species of fishes caught in a fishing area of the South Adriatic Sea. A host-parasite list is given. Twenty species of fish were analysed and twenty-seven species of digeneans were found, twenty of which had previously been described in the same host, and six of which were observed in new hosts and/or localities. One digenean, hitherto undescribed, is illustrated in this paper and described as Lecithaster atherinae n.sp. The new species can be distinguished from L. bombayensis by the testes not being lobed; from L. extralobus by having four rather than five ovarian lobes; from L. indicus and L. maeoticus by the ovarian lobes not being finger-like; from L. leiostomi by having definitely smaller eggs.     

Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea.

An important component of the parasite fauna of seabirds in arctic regions are the flukes (Digena). Different species of digeneans have life cycles which may consist of 1 intermediate host and no free-living larval stages, 2 intermediate hosts and 1 free-living stage, or 2 intermediate hosts and 2 free-living larval stages. This study examined the distribution of such parasites in the intertidal zones of the southern coast of the Barents Sea (northwestern Russia and northern Norway) by investigating 2 species of periwinkles (Littorina saxatilis and L. obtusata) which are intermediate hosts of many species of digeneans. A total of 26,020 snails from 134 sampling stations were collected. The study area was divided into 5 regions, and the number of species, frequency of occurrence and prevalence of different digenean species and groups of species (depending on life cycle complexity) were compared among these regions, statistically controlling for environmental exposure. We found 14 species of digeneans, of which 13 have marine birds as final hosts. The number of species per sampling station increased westwards, and was higher on the Norwegian coast than on the Russian coast. The frequency of occurrence of digeneans with more than 1 intermediate host increased westwards, making up a larger proportion of the digeneans among infected snails. This was significant in L. saxatilis. The prevalence of different species showed the same pattern, and significantly more snails of both species were infected with digeneans with complicated life cycles in the western regions. In L. saxatilis, environmental exposure had a statistically significant effect on the distribution of the most common digenean species. This was less obvious in L. obtusata. The causes of changing species composition between regions are probably (1) the harsh climate in the eastern part of the study area reducing the probability of successful transmission of digeneans with complicated life cycles, and (2) the distribution of different final hosts.     

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.