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A Model for Evolutionary Ecology of Disease: The Case for Caenorhabditis Nematodes and Their Natural Parasites

AMANDA K. GIBSON
AMANDA K. GIBSON
 and 
LEVI T. MORRAN
LEVI T. MORRAN
   | Sep 26, 2018
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Published Online: Sep 26, 2018
Page range: 357 - 372
Received: Feb 22, 2017
DOI: https://doi.org/10.21307/jofnem-2017-083
Keywords
© 2017 AMANDA K. GIBSON published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

FIG. 1.

Fungal parasite species richness as a function of study effort for hosts in the Brassicales. Host taxa were obtained from the Brassicales phylogeny in Beilstein et al. (2010, Fig. S1). Study effort is the number of citations obtained by copying and pasting a host’s full name, in quotations, in Google Scholar. Parasite species richness is the number of fungal parasite species reported infecting a host in the USDA Fungus-Host Database (https://nt.ars-grin.gov/fungaldatabases/). There is a positive correlation between study effort (citation number, untransformed) and parasite species richness, with (Spearman rank correlation, ρ = 0.772, P < 0.001) and without (ρ = 0.767, P < 0.001) the uppermost point (Brassica oleracea) (tests exclude Arabidopsis thaliana).
Fungal parasite species richness as a function of study effort for hosts in the Brassicales. Host taxa were obtained from the Brassicales phylogeny in Beilstein et al. (2010, Fig. S1). Study effort is the number of citations obtained by copying and pasting a host’s full name, in quotations, in Google Scholar. Parasite species richness is the number of fungal parasite species reported infecting a host in the USDA Fungus-Host Database (https://nt.ars-grin.gov/fungaldatabases/). There is a positive correlation between study effort (citation number, untransformed) and parasite species richness, with (Spearman rank correlation, ρ = 0.772, P < 0.001) and without (ρ = 0.767, P < 0.001) the uppermost point (Brassica oleracea) (tests exclude Arabidopsis thaliana).

FIG. 2.

Natural parasites of Caenorhabditis elegans. A. The taxonomic distribution of unnatural parasites of C. elegans. These are parasites paired with C. elegans in the laboratory that are not presently known to infect C. elegans in the wild. The parasites are identified in Sifri et al. (2005, Table 1). Unlike in Sifri et al. (2005), we did not include Microbacterium nematophilum and Drechmeria coniospora here, because we treated these as natural parasites. See our Table 1 for more details. B. The taxonomic distribution of known natural parasites of C. elegans. These are parasites known, or strongly suspected, to facultatively or obligately associate with C. elegans in the wild and depress fitness. The parasites are listed in Table 1, with descriptive details and citations. These are only the parasites that have been reported in sufficient detail to characterize the nature of their association with C. elegans. Further study will certainly uncover more species. The sizes of the pie charts are scaled to the number of total taxa.
Natural parasites of Caenorhabditis elegans. A. The taxonomic distribution of unnatural parasites of C. elegans. These are parasites paired with C. elegans in the laboratory that are not presently known to infect C. elegans in the wild. The parasites are identified in Sifri et al. (2005, Table 1). Unlike in Sifri et al. (2005), we did not include Microbacterium nematophilum and Drechmeria coniospora here, because we treated these as natural parasites. See our Table 1 for more details. B. The taxonomic distribution of known natural parasites of C. elegans. These are parasites known, or strongly suspected, to facultatively or obligately associate with C. elegans in the wild and depress fitness. The parasites are listed in Table 1, with descriptive details and citations. These are only the parasites that have been reported in sufficient detail to characterize the nature of their association with C. elegans. Further study will certainly uncover more species. The sizes of the pie charts are scaled to the number of total taxa.

Natural parasites of Caenorhabditis elegans. The list comprises parasites that are confirmed or strongly suspected to infect C. elegans and related hosts in the wild. Parasites are lethal to their hosts unless otherwise indicated.

Species Infection site Obligate? Phylogenetic context Citation
Microsporidia
Nematocida parisii Intestinal cells Yes Zhang et al. (2016) describe many species of Nematocida infecting rhabditid nematodes. They also describe two new genera of microsporidia infecting nematodes of the genus Oscheius. Troemel et al. (2008)
   Nematocida ausubeli Intestinal cells Yes Troemel et al. (2008), Zhang et al. (2016)
   Nematocida ironsii Intestinal cells Yes Reinke et al. (2017)
   Nematocida displodere Systemic: primarily muscle and epidermis Yes Luallen et al. (2016)
Viruses
   Orsay virus Intestinal cells Yes Caenorhabditis briggsae is infected by close relatives, the LeBlanc and Santeuil viruses (Felix et al., 2011; Franz et al., 2012, 2014). All these viruses are distantly related to nodaviruses. Felix et al. (2011)
Fungi
   Harposporium sp. Systemic: nematophagous members of the genus establish in the intestine or on the cuticle, then produce hyphae that invade the entire body Likely: endoparasitic species can grow outside the host, but there is no evidence that they do so in nature Species of Harposporium are found infecting nematodes of many genera, including Acrobeles, Panagrellus, Bunonema, and Aphelenchoices (Esser and El-Gholl, 1992). Félix and Duveau (2012)
   Drechmeria coniospora Systemic: adheres to the cuticle, frequently around the mouth, then hyphae invade the entire body Yes A model fungal parasite of C. elegans. Drechmeria coniospora was identified as a natural parasite after it was found infecting C. briggsae in the wild (Félix and Duveau, 2012). It can infect a broad range of nematode species (Jansson and Nordbring-Hertz, 1983), suggesting that it likely infects C. elegans naturally. Jansson et al. (1985), Jansson (1994), Félix and Duveau (2012)
Bacteria
   Leucobacter musarum japonicus a Rectal, postanal Likely facultative b This species is very similar to a related coryneform bacteria, Microbacterium nematophilum, which infects laboratory cultures of C. elegans (Hodgkin et al., 2000). Leucobacter musarum subsp. musarum and a related species (Leucobacter celer) were found naturally infecting an unidentified Caenorhabditis sp. (Hodgkin et al., 2013; Clark and Hodgkin, 2015). Hodgkin et al. (2013)
   Elizabethkingia sp. c Systemic: dissolves nematode cuticle Likely facultative b      Félix and Duveau (2012)
   Chryseobacterium sp. a,b Not described Likely facultative b This genus is closely related to Elizabethkingia (Bernardet et al., 2006) Samuel et al. (2016)
   Serratia sp. c Not described Likely facultative b Serratia species are facultative parasites of humans, plants, and invertebrates (corals, nematodes, and insects) and occasionally mutualists or various hosts (plants, nematodes, and aphids) (Petersen and Tisa, 2013). Serratia marcescens infection of C. elegans is commonly studied in the laboratory, al though this species is not known to cause infection in the wild. Samuel et al. (2016)
   Pseudomonas sp. c Not described Likely facultative b Pseudomonas species are widespread in the environment and cause infection in a diversity of hosts, including plants and humans. Particular strains of P. aeruginosa infect C. elegans in the laboratory. Samuel et al. (2016)
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