Concepts in Animal Parasitology, Chapter 57: Nematomorpha (Phylum): Horsehair Worms

Chapter 57 in Concepts in Animal Parasitology on the horsehair worms, phylum Nematomorpha, by Matthew G. Bolek and Ben Hanelt. 2024. S. L. Gardner and S. A. Gardner, editors. Zea Books, Lincoln, Nebraska, United States. doi: 10.32873/unl.dc.ciap05

Physid Snails as Sentinels of Freshwater Nematomorphs

Freshwater nematomorphs, or gordiids, are parasitic as larvae, but free-living in aquatic environments as adults. Studies based on the collection of adults have reported gordiids to be widespread, but discontinuous in distribution. However, a relatively short adult life span and unknown life history make the detection of adults difficult. An alternative approach to investigate gordiid distribution is to use cysts. Of all paratenic hosts, snails were chosen because they lacked internal defense reactions to the cysts and become easily infected. Here, it is reported that the occurrence of gordiids on the basis of the cyst stage is much more common than previously reported, thus altering the perception of how common these worms are. Using this modified survey procedure, gordiid cysts were found at 70% of sites examined, in an area where extensive sampling over 3 yr yielded adults only at a single site. Of 1,000 snails dissected, 395 were infected with gordiids (intensity range: 1-465). Furthermore, different types of human-modified landscapes did not affect gordiid distribution, suggesting that as urban and suburban areas sprawl, human encounters or pseudoparasitism with nematomorphs may increase. The results of this study indicate that use of organismal-specific sampling techniques can be critical in studies of parasite distribution and biodiversity

Physid Snails as Sentinels of Freshwater Nematomorphs

Freshwater nematomorphs, or gordiids, are parasitic as larvae, but free-living in aquatic environments as adults. Studies based on the collection of adults have reported gordiids to be widespread, but discontinuous in distribution. However, a relatively short adult life span and unknown life history make the detection of adults difficult. An alternative approach to investigate gordiid distribution is to use cysts. Of all paratenic hosts, snails were chosen because they lacked internal defense reactions to the cysts and become easily infected. Here, it is reported that the occurrence of gordiids on the basis of the cyst stage is much more common than previously reported, thus altering the perception of how common these worms are. Using this modified survey procedure, gordiid cysts were found at 70% of sites examined, in an area where extensive sampling over 3 yr yielded adults only at a single site. Of 1,000 snails dissected, 395 were infected with gordiids (intensity range: 1-465). Furthermore, different types of human-modified landscapes did not affect gordiid distribution, suggesting that as urban and suburban areas sprawl, human encounters or pseudoparasitism with nematomorphs may increase. The results of this study indicate that use of organismal-specific sampling techniques can be critical in studies of parasite distribution and biodiversity

The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from Biomphalaria glabrata.

BackgroundThe full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used.Principal findingsTranscripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity.Conclusions/significanceThis in vivo study, emphasizing field-derived snails and schistosomes, but supplemented with observations from a lab model, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be elucidated

A New Species of \u3ci\u3eGordius\u3c/i\u3e (Phylum Nematomorpha) from Terrestrial Habitats in North America

Freshwater hairworms (class Gordiida) are members of the phylum Nematomorpha that use terrestrial arthropods as definitive hosts but reside as free-living adult worms in rivers, lakes, or streams. The genus Gordius consists of 90 described species, of which three species were described from freshwater habitats in North America. In this paper we describe a new species of Gordius from terrestrial habitats in Oklahoma, Texas, and Louisiana, United States. Oddly, each year hundreds of adult free-living worms appear after bouts of heavy rain on streets, sidewalks, and lawns during the winter season, when terrestrial arthropod hosts are not active. The new species is described based on morphological characters of adults and nonadult stages including the egg strings, eggs, larvae, and cysts. Adult males have a unique row of bristles on the ventral inner side of each tail lobe and a circular pattern of bristles on the terminal end of each lobe, which distinguishes them from all other described North American species of Gordius. The egg string, larval, and cyst morphology of this new species conform to previous descriptions of non-adult hairworm stages for the genus Gordius. However, the eggs of this new species of hairworm are unique, as they contain an outer shell separated by distinct space from a thick inner membrane. The consistent occurrence of this gordiid in terrestrial habitats, along with its distinct egg morphology, suggests that this new species of hairworm has a terrestrial life cycle

Two New Species and Temporal Changes in the Prevalence of Eimerians in a Free-Living Population of Townsend\u27s Ground Squirrels (\u3ci\u3eSpermophilus townsendii\u3c/i\u3e) in Idaho

More than 1,180 fecal samples were collected from 253 juvenile and 384 adult Townsend\u27s ground squirrels (Spermophilus townsendii) at the Snae Snake River Birds of Prey Area near Boise, Idaho, from February to June 1992. Oocysts of 7 eimerians were observed. Five are new host records (Eimeria beecheyi, Eimeria bilamellata, Eimeria callospermophili, Eimeria lateralis, and Eimeria morainensis), 2 species are described here as new, and new structural information on E. morainensis is added. Sporulated oocysts of Eimeria adaensis n. sp. are ovoidal, 19.6 x 22.7 (16-22 x 18-26) μm with sporocysts ellipsoidal 7.2 x 11.9 (6-10 x 9-15) μm. No micropyle or oocyst residuum, but polar bodies, Stieda bodies, and sporocyst residua are present. Sporulated oocysts of Eimeria pseudospermophili n. sp. are ovoidal, 24.7 x 28.5 (21-27 x 25-32) μm with sporocysts ellipsoidal 8.8 x 14.2 (8-10 x 12-17) μm. Micropyle and oocyst residuum are absent, but polar bodies and Stieda bodies are present. Sporulated oocysts of E. morainensis are more variable in size and shape than originally described and contain 2 distinctly different residua not previously described. Temporal changes in the prevalence of eimerians of all 7 species combined in adult squirrels showed significant decline (r2 = 0.79, P \u3c 0.001). We hypothesize that this decline was due to drought during the period of squirrel activity. No significant temporal change in the prevalence of eimerians in juvenile squirrels was observed. The prevalence of E. callospermophili, E. adaensis, and all eimerians combined in adults was significantly greater than in juveniles. There was no significant difference in eimerian prevalence between male and female squirrels (P \u3c 0.05)

Going Solo: Discovery of the First Parthenogenetic Gordiid (Nematomorpha: Gordiida)

Despite the severe fitness costs associated with sexual reproduction, its persistence and pervasiveness among multicellular organisms testifies to its intrinsic, short-term advantages. However, the reproductive assurance hypothesis predicts selection favoring asexual reproduction in sparse populations and when mate finding is difficult. Difficulties in finding mates is especially common in parasites, whose life cycles involve multiple hosts, or being released from the host into the external environment where the parasite can find itself trapped without a sexual partner. To solve this problem and guarantee reproduction, parasites in numerous phyla have evolved reproductive strategies, as predicted by the reproductive assurance hypothesis, such as hermaphroditism or parthenogenesis. However, this type of strategy has not been reported from species in the phylum Nematomorpha, whose populations have often been described as sparse. A new Nematomorpha species, Paragordius obamai n. sp., was discovered from Kenya, Africa, and appears to have solved the problem of being trapped without a mate by eliminating the need for males. Paragordius obamai n. sp. represents the first and only known species within this phylum to reproduce asexually. To determine the mechanism of this mating strategy, we ruled out the involvement of reproduction manipulating endosymbionts by use of next generation sequencing data, thus suggesting that parthenogenesis is determined genetically and may have evolved as a means to assure reproduction. Since this new parthenogenetic species and a closely related gonochoristic North American congener, P. varius, are easy to propagate in the laboratory, these gordiids can be used as model systems to test hypotheses on the genetic advantages and disadvantages of asexual reproduction and the genetic determinants of reproductive strategies in parasites

Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages.

Small RNA pathways act at the front line of defence against transposable elements across the Eukaryota. In animals, Piwi interacting small RNAs (piRNAs) are a crucial arm of this defence. However, the evolutionary relationships among piRNAs and other small RNA pathways targeting transposable elements are poorly resolved. To address this question we sequenced small RNAs from multiple, diverse nematode species, producing the first phylum-wide analysis of how small RNA pathways evolve. Surprisingly, despite their prominence in Caenorhabditis elegans and closely related nematodes, piRNAs are absent in all other nematode lineages. We found that there are at least two evolutionarily distinct mechanisms that compensate for the absence of piRNAs, both involving RNA-dependent RNA polymerases (RdRPs). Whilst one pathway is unique to nematodes, the second involves Dicer-dependent RNA-directed DNA methylation, hitherto unknown in animals, and bears striking similarity to transposon-control mechanisms in fungi and plants. Our results highlight the rapid, context-dependent evolution of small RNA pathways and suggest piRNAs in animals may have replaced an ancient eukaryotic RNA-dependent RNA polymerase pathway to control transposable elements.We thank Sylviane Moss for high-throughput sequencing support. We thank Charles Bradshaw for help with computation and IT. We thank Marie-Anne Felix and Frank Jiggins for critical comments on the manuscript. We thank Matt Berriman (Wellcome Trust Sanger Centre, Hinxton, Cambridge, UK) for allowing us to use unpublished genomic sequencing data for N. brasiliensis. We thank Einhardt Schierenberg (University of Cologne, Germany) and Werner Armonies (Alfred Wegener Institute, Sylt, Germany) for help with collection of E. brevis.This is the final version of the article, originally published in PLoS Biology, 2015, 13(2): e1002061. doi:10.1371/journal.pbio.100206

Concepts in Animal Parasitology, Part 4: Nemata, Nematomorpha, Acanthocephala, Pentastomida

Part IV: Nemata, Nematomorpha, Acanthocephala, Pentastomida, chapters 48-59, pages 532-, in Concepts in Animal Parasitology. 2024. Scott L. Gardner and Sue Ann Gardner, editors. Zea Books, Lincoln, Nebraska, United States; part IV doi: 10.32873/unl.dc.ciap074 Nemata: Endoparasitic Nematodes Chapter 48: Introduction to Endoparasitic Nematodes (Phylum Nemata) by Scott L. Gardner, pages 533-544 Chapter 49: Trichuroidea and Trichinelloidea (Superfamilies) by María del Rosario Robles and Rocío Callejón Fernández, pages 545-565 Chapter 50: Ascaridoidea (Superfamily): Large Intestinal Nematodes by Larry S. Roberts, John J. Janovy, Jr., Steven Nadler, and Scott L. Gardner, pages 566-581 Chapter 51: Heterakoidea (Superfamily): Cosmopolitan Gut-Dwelling Parasites of Tetrapods by F. Agustín Jiménez-Ruiz, pages 582-592 Chapter 52: Oxyurida (Order): Pinworms by Haylee J. Weaver, pages 593-599 Chapter 53: Spirurida (Order) by Valentin Radev, pages 600-624 Chapter 54: Camallanina (Suborder): Guinea Worm and Related Nematodes by Anindo Choudhury, pages 625-632 Chapter 55: Filarioidea (Superfamily) by Juliana Notarnicola, pages 633-655 Chapter 56: Strongyloidea and Trichostrongyloidea (Superfamilies): Bursate Nematodes by Larry S. Roberts, John J. Janovy, Jr., Steven Nadler, Valentin Radev, and Scott L. Gardner, pages 656-679 Nematomorpha Chapter 57: Nematomorpha (Phylum): Horsehair Worms by Matthew G. Bolek and Ben Hanelt, pages 681-698 Acanthocephala Chapter 58: Acanthocephala (Phylum) by Scott Monks, pages 700-714 Pentastomida Chapter 59: Pentastomida: Endoparasitic Arthropods by Chris T. McAllister, pages 716-73