The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by high species diversity. This inspired us to examine the history of adaptive radiations in myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes, and the Myxozoa, and proposed fish as original hosts for both sister lineages. We demonstrate that the Myxozoa emerged long before fish populated Earth and that phylogenetic congruence with their invertebrate hosts is evident down to the most basal branches of the tree, indicating bryozoans and annelids as original hosts and challenging previous evolutionary hypotheses. We provide evidence that, following invertebrate invasion, fish hosts were acquired multiple times, leading to parallel cospeciation patterns in all major phylogenetic lineages. We identify the acquisition of vertebrate hosts that facilitate alternative transmission and dispersion strategies as reason for the distinct success of the Myxozoa, and identify massive host specification-linked parasite diversification events. The results of this study transform our understanding of the origins and evolution of parasitism in the most basal metazoan parasites known.
Infectious diseases are contributing to the decline of endangered amphibians. We identified myxosporean parasites, Myxidium spp. (Myxosporea: Myxozoa), in the brain and liver of declining native frogs, the Green and Golden Bell frog (Litoria aurea) and the Southern Bell frog (Litoria raniformis). We unequivocally identified two Myxidium spp. (both generalist) affecting Australian native frogs and the invasive Cane toad (Bufo marinus, syn. Rhinella marina) and demonstrated their association with disease. Our study tested the identity of Myxidium spp. within native frogs and the invasive Cane toad (brought to Australia in 1935, via Hawaii) to resolve the question whether the Cane toad introduced them to Australia. We showed that the Australian brain and liver Myxidium spp. differed 9%, 7%, 34% and 37% at the small subunit rDNA, large subunit rDNA, internal transcribed spacers 1 and 2, but were distinct from Myxidium cf. immersum from Cane toads in Brazil. Plotting minimum within-group distance against maximum intra-group distance confirmed their independent evolutionary trajectory. Transmission electron microscopy revealed that the brain stages localize inside axons. Myxospores were morphologically indistinguishable, therefore genetic characterisation was necessary to recognise these cryptic species. It is unlikely that the Cane toad brought the myxosporean parasites to Australia, because the parasites were not found in 261 Hawaiian Cane toads. Instead, these data support the enemy-release hypothesis predicting that not all parasites are translocated with their hosts and suggest that the Cane toad may have played an important spill-back role in their emergence and facilitated their dissemination. This work emphasizes the importance of accurate species identification of pathogens relevant to wildlife management and disease control. In our case it is paving the road for the spill-back role of the Cane toad and the parasite emergence.
Parasites are often hidden in their hosts and exhibit patchy spatial distributions. This makes them relatively difficult to detect and sample. Consequently we have poor knowledge of parasite diversities, distributions and extinction. We evaluate our general understanding of parasite diversity and highlight the enormous bias in research on parasites such as helminths and arthropods that infect vertebrate hosts. We then focus on Myxozoa as an exemplary case for demonstrating uncharted parasite diversity. Myxozoans are a poorly recognised but speciose clade of endoparasitic cnidarians with complex life cycles that have radiated to exploit freshwater, marine and terrestrial hosts by adopting strategies convergent to those of parasitic protists. Myxozoans are estimated to represent some 20% of described cnidarian species - greatly outnumbering the combined species richness of scyphozoans, cubozoans, and staurozoans. We summarise limited understanding of myxozoan diversification and geographical distributions, and highlight gaps in knowledge and approaches for measuring myxozoan diversity. We close by reviewing methods and problems in estimating parasite extinction and concerns about extinction risks in view of the fundamental roles parasites play in ecosystem dynamics and in driving host evolutionary trajectories.
Two new myxosporean species in the gallbladders of frogs have recently spread across eastern Australia and cause disease. Cystodiscus axonis sp. n. and Cystodiscus australis sp. n. are species of Myxosporea (Myxozoa) identified from a range of Australian frogs and tadpoles including the introduced Cane toad (Rhinella marina). The new species are defined by their distinct genetic lineage, myxospore morphology and ultrastructure of the pre-sporogonic development. Spores of both species are produced in the gallbladder. Spores of C. axonis sp. n. possess distinct filiform polar appendages (FPA). The pre-sporogonic development of C. axonis sp. n. is within myelinated axons in the central nervous system of hosts, as well as bile ducts of tadpoles. Pre-sporogonic and sporogonic development of C. australis sp. n. is confined to tadpole bile ducts and myxospores of C. australis sp. n. are devoid of FPA. The genus Cystodiscus Lutz, 1889 introduced for Cystodiscus immersus Lutz, 1889 is emended to accompany myxosporean parasites affecting amphibians previously classified in the genus Myxidium sensu lato. A synopsis of described species within Cystodiscus is provided.
BackgroundA parasite morphologically indistinguishable from Myxidium immersum (Myxozoa: Myxosporea) found in gallbladders of the invasive cane toad (Bufo marinus) was identified in Australian frogs. Because no written record exists for such a parasite in Australian endemic frogs in 19th and early 20th century, it was assumed that the cane toad introduced this parasite. While we cannot go back in time ourselves, we investigated whether material at the museum of natural history could be used to retrieve parasites, and whether they were infected at the time of their collection (specifically prior to and after the cane toad translocation to Australia in 1935).ResultsUsing the herpetological collection at the Australian Museum we showed that no myxospores were found in any animals (n = 115) prior to the cane toad invasion (1879-1935). The green and golden bell frog (Litoria aurea), the Peron's tree frog (Litoria peronii), the green tree frog (Litoria caerulea) and the striped marsh frog (Limnodynastes peronii) were all negative for the presence of the parasite using microscopy of the gallbladder content and its histology. These results were sufficient to conclude that the population was free from this disease (at the expected minimum prevalence of 5%) at 99.7% confidence level using the 115 voucher specimens in the Australian Museum. Similarly, museum specimens (n = 29) of the green and golden bell frog from New Caledonia, where it was introduced in 19th century, did not show the presence of myxospores. The earliest specimen positive for myxospores in a gallbladder was a green tree frog from 1966. Myxospores were found in eight (7.1%, n = 112) frogs in the post cane toad introduction period.ConclusionAustralian wildlife is increasingly under threat, and amphibian decline is one of the most dramatic examples. The museum material proved essential to directly support the evidence of parasite emergence in Australian native frogs. This parasite can be considered one of the luckiest parasites, because it has found an empty niche in Australia. It now flourishes in > 20 endemic and exotic frog species, but its consequences are yet to be fully understood.
Cellular motility is essential for microscopic parasites, it is used to reach the host, migrate through tissues, or evade host immune reactions. Many cells employ an evolutionary conserved motor protein– actin, to crawl or glide along a substrate. We describe the peculiar movement of Sphaerospora molnari, a myxozoan parasite with proliferating blood stages in its host, common carp. Myxozoa are highly adapted parasitic cnidarians alternately infecting vertebrates and invertebrates. S. molnari blood stages (SMBS) have developed a unique “dancing” behaviour, using the external membrane as a motility effector to rotate and move the cell. SMBS movement is exceptionally fast compared to other myxozoans, non-directional and constant. The movement is based on two cytoplasmic actins that are highly divergent from those of other metazoans. We produced a specific polyclonal actin antibody for the staining and immunolabelling of S. molnari’s microfilaments since we found that neither commercial antibodies nor phalloidin recognised the protein or microfilaments. We show the in situ localization of this actin in the parasite and discuss the importance of this motility for evasion from the cellular host immune response in vitro. This new type of motility holds key insights into the evolution of cellular motility and associated proteins.
Myxozoans are widespread and common endoparasites of fish with complex life cycles, infecting vertebrate and invertebrate hosts. There are two classes: Myxosporea and Malacosporea. To date about 2500 myxosporean species have been described. By comparison, there are only five described malacosporean species. Malacosporean development in the invertebrate hosts (freshwater bryozoans) has been relatively well studied but is poorly known in fish hosts. Our aim was to investigate the presence and development of malacosporeans infecting a diversity of fish from Brazil, Europe and the USA. We examined kidney from 256 fish belonging variously to the Salmonidae, Cyprinidae, Nemacheilidae, Esocidae, Percidae, Polyodontidae, Serrasalmidae, Cichlidae and Pimelodidae. Malacosporean infections were detected and identified by polymerase chain reaction and small subunit ribosomal DNA sequencing, and the presence of sporogonic stages was evaluated by ultrastructural examination. We found five malacosporean infections in populations of seven European fish species (brown trout, rainbow trout, white fish, dace, roach, gudgeon and stone loach). Ultrastructural analyses revealed sporogonic stages in kidney tubules of three fish species (brown trout, roach and stone loach), providing evidence that fish belonging to at least three families are true hosts. These results expand the range of fish hosts exploited by malacosporeans to complete their life cycle.
Experimental infections of Sminthopsis crassicaudata, the fat-tailed dunnart, a carnivorous marsupial widely distributed throughout the arid and semi-arid zones of Australia, show that this species can act as an intermediate host for Neospora caninum. In contrast to existing models that develop relatively few N. caninum tissue cysts, dunnarts offer a new animal model in which active neosporosis is dominated by tissue cyst production. The results provide evidence for a sylvatic life cycle of N. caninum in Australia between marsupials and wild dogs. It establishes the foundation for an investigation of the impact and costs of neosporosis to wildlife.
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