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The Evolution of Uniparental Reproduction in Rhabditina Nematodes: Phylogenetic Patterns, Developmental Causes, and Surprising Consequences

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Transitions Between Sexual Systems

Abstract

Many groups of eukaryotes with an ancestrally outcrossing sexual system include species that have adopted uniparental reproduction (either parthenogenesis or self-fertility). Nematodes are one such group. Because of recent advances in molecular phylogenetics, the evolutionary patterns of nematode sexual mode are becoming clearer. In this chapter, we first present a molecular phylogeny of over 200 Clade 9 nematodes and map changes in sexual mode upon it. Clade 9 includes both parasites of the order Strongylida and free-living species that include Caenorhabditis elegans, the most studied nematode. Uniparental reproduction has evolved a minimum of 15 times in the clade, but none of these are within the clade of parasitic species. We discern two local phylogenetic patterns after the origin of uniparental reproduction. In Pattern 1, parthenogenic or selfing species are isolated taxa that apparently go extinct before speciation. In Pattern 2, uniparental reproduction is ancestral to a diversified clade and is relatively ancient. We next review the evolutionary developmental biology aspects of self-fertility in Caenorhabditis, the one taxon for which it has been investigated. Finally, we summarize recent work documenting surprising impacts of self-fertility on genome size and content.

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References

  • Abolafia J (2006) Chapter 22: Order Rhabditida, Suborder Rhabditina. In: Abebe E, Andrassy I, Truanspurger W (eds) Freshwater nematodes: ecology and taxonomy. CABI, Oxfordshire, UK

    Google Scholar 

  • Andrássy I (1983) A taxonomic review of the suborder Rhabditina (Nematoda: Secernentia). Orstom, Paris

    Google Scholar 

  • Bai X, Adams BJ, Ciche TA, Clifton S, Gaugler R, Kim KS, Spieth J, Sternberg PW, Wilson RK, Grewal PS (2013) A lover and a fighter: the genome sequence of an entomopathogenic nematode Heterorhabditis bacteriophora. PLoS One 8:e69618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker MR (1979) The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidae) in amphibians. Can J Zool 57:161–178

    Article  Google Scholar 

  • Baldi C, Cho S, Ellis RE (2009) Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326:1002–1005

    Article  CAS  PubMed  Google Scholar 

  • Barrett SC (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284

    Article  CAS  PubMed  Google Scholar 

  • Baylis H, Daubney R (1925) A revision of the lung-worms of Cetacea. Parasitology 17(2):201–215

    Article  Google Scholar 

  • Beadell AV, Liu Q, Johnson DM, Haag ES (2011) Independent recruitments of a translational regulator in the evolution of self-fertile nematodes. Proc Natl Acad Sci USA 108:19672–19677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beveridge I (1979) Hypodontus macropi Monnig, 1929, a hookworm-like parasite of macropodid marsupials. J Helminthol 53(3):229–244

    Article  CAS  PubMed  Google Scholar 

  • Beveridge I, Durett-Desset M-C (1986) New species of Austrostrongylus Chandler, 1924 (Nematoda, Trichostrongyloidea), from Australian Marsupials, with a redescription of A. minutus Johnston & Mawson, 1938, and description of a new genus, Sutarostrongylus. Bull Mus Natl Hist Nat Paris 8:145–170

    Google Scholar 

  • Bhaibulaya M, Cross JH (1971) Angiostrongylus malaysiensis (Nematoda: Metastrongylidae), a new species of rat lung-worm from Malaysia. Southeast Asian J Trop Med Public Health 2(4):527–533

    CAS  PubMed  Google Scholar 

  • Bongers T, Vereniging KNN, Vereniging KNN (1988) De Nematoden van Nederland: Een identificatietabel voor de in Nederland aangetroffen zoetwater-en bodembewonende nematoden. Koninklijke Nederlandse Natuurhistorische Vereiniging, Utrecht

    Google Scholar 

  • Bowman D, Hendrix C, Lindsay D, Barr S (2002) Feline clinical parasitology. Iowa State University Press, Ames, IA

    Book  Google Scholar 

  • Brandvain Y, Haig D (2005) Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am Nat 166:330–338

    Article  PubMed  Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brenner S (2009) In the beginning was the worm. Genetics 182:413–415

    Article  PubMed  PubMed Central  Google Scholar 

  • Calaway W, Tarjan A (1973) A compendium of the genus Mononchoides Rahm, 1928 (Diplogastrinae: Nematoda). J Nematol 5(2):107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Camberis M, Le Gros G, Urban J Jr (2003) Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr Protoc Immunol Chapter 19 Unit 19:12

    Google Scholar 

  • Cameron TW, Myers BJ (1961) On a phylogenetic classification of the Family Trichostrongylidae Leiper of Marsupials, Insectivores and Edentates. J Helminthol 35(S1):25–34

    Article  Google Scholar 

  • Carta LK, Osbrink W (2005) Rhabditis rainai n. sp.(Nematoda: Rhabditida) associated with the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae). Nematology 7(6):863–879

    Article  Google Scholar 

  • Chaudhuri J, Kache V, Pires-daSilva A (2011) Regulation of sexual plasticity in a nematode that produces males, females, and hermaphrodites. Curr Biol 21:1548–1551

    Article  CAS  PubMed  Google Scholar 

  • Chen PJ, Cho S, Jin SW, Ellis RE (2001) Specification of germ cell fates by FOG-3 has been conserved during nematode evolution. Genetics 158:1513–1525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chilton NB, Huby-Chilton F, Gasser RB (2003) First complete large subunit ribosomal RNA sequence and secondary structure for a parasitic nematode: phylogenetic and diagnostic implications. Mol Cell Probes 17(1):33–39

    Article  CAS  PubMed  Google Scholar 

  • Chilton NB, Huby-Chilton F, Gasser RB, Beveridge I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Mol Phylogenet Evol 40(1):118–128

    Article  CAS  PubMed  Google Scholar 

  • Chitambar J, Noffsinger EM (1989) Taxonomy and postembryonic stages of the nematode predator Odontopharynx longicaudata de Man, 1912 (Diplogasterida). J Nematol 21(2):189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho S, Jin SW, Cohen A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14:1207–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciche T (2007) The biology and genome of Heterorhabditis bacteriophora (February 20, 2007) In: Wormbook, The C. elegans Research Community (ed)

    Google Scholar 

  • Clifford R, Lee M, Nayak S, Ohmachi M, Giorgini F, Schedl T (2000) FOG-2, a novel F-box-containing protein, associates with the GLD-1 RNA-binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127:5265–5276

    CAS  PubMed  Google Scholar 

  • Cobb N (1920) One hundred new nemas. Contributions to a science of nematology 9:217–343

    Google Scholar 

  • Costa JO, de Araujo Costa HM, Guimaraes MP (2003) Redescription of Angiostrongylus vasorum (Baillet, 1866) and systematic revision of species assigned to the genera Angiostrongylus Kamensky, 1905 and Angiocaulus Schulz, 1951. Rev Med Vet 154:9–16

    Google Scholar 

  • Cutter AD (2006) Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics 172:171–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutter AD (2008) Reproductive evolution: symptom of a selfing syndrome. Curr Biol 18:R1056–R1058

    Article  CAS  PubMed  Google Scholar 

  • Cutter AD, Baird SE, Charlesworth D (2006) High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics 174:901–913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dailey MD (2009) A new species of Parafilaroides (Nematoda: Filaroididae) in three species of fur seals (Carnivora: Otariidae) from the Southern Hemisphere. J Parasitol 95(1):156–159

    Article  PubMed  Google Scholar 

  • Davis MP, Midford PE, Maddison W (2013) Exploring power and parameter estimation of the BiSSE method for analyzing species diversification. BMC Evol Biol 13:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Denver DR, Clark KA, Raboin MJ (2011) Reproductive mode evolution in nematodes: insights from molecular phylogenies and recently discovered species. Mol Phylogenet Evol 61:584–592

    Article  CAS  PubMed  Google Scholar 

  • Dey A, Chan CK, Thomas CG, Cutter AD (2013) Molecular hyperdiversity defines populations of the nematode Caenorhabditis brenneri. Proc Natl Acad Sci USA 110:11056–11060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Divina BP, Wilhelmsson E, Mattsson JG, Waller P, Hoglund J (2000) Identification of Dictyocaulus spp. in ruminants by morphological and molecular analyses. Parasitology 121(Pt 2):193–201

    Article  PubMed  Google Scholar 

  • Drozdz J, Doby JM, Mandahl-Barth G (1971) [Study of the morphology and larval development of Angiostrongylus (Parastrongylus) dujardini Drozdz and Doby 1970, Nematoda: Metastrongyloiidea Infestation of the molluscan intermediary hosts]. Ann Parasitol Hum Comp 46(3), 265–276

    Google Scholar 

  • Durett-Desset M-C (2009) Chapter 6: Strongylida—Trychostrongyloidea. In: Anderson R, Chabaud A, Willmott S (eds) Keys to the nematode parasites of vertebrates: archival volume. CABI, Oxfordshire, UK

    Google Scholar 

  • Durette-Desset M, Cassone J (1983) A taxonomic revision of the Trichostrongyloid Nematode Parasites of the Echidna, Tachyglossus Aculeatus (Monotremata). Aust J Zool 31(2):257–284

    Article  Google Scholar 

  • Ehlers R-U, Lunau S, Krasomil-Osterfeld K, Osterfeld KH (1998) Liquid culture of the entomopathogenic nematode-bacterium-complex Heterorhabditis megidis/Photorhabdus luminescens. BioControl 43(1):77–86

    Article  Google Scholar 

  • Eira C, Torres J, Vingada J, Miquel J (2006) Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus. Acta Parasitol 51:300–308

    Google Scholar 

  • Ellis RE (2008) Sex determination in the Caenorhabditis elegans germ line. Curr Top Dev Biol 83:41–64

    Article  CAS  PubMed  Google Scholar 

  • Ellis RE, Lin SY (2014) The evolutionary origins and consequences of self-fertility in nematodes. F1000Prime Rep 6:62

    Google Scholar 

  • Faulkner J, Measures L, Whoriskey F (1998) Stenurus minor (Metastrongyloidea: Pseudaliidae) infections of the cranial sinuses of the harbour porpoise, Phocoena phocoena. Can J Zool 76:1209–1216

    Article  Google Scholar 

  • Felix MA (2004) Alternative morphs and plasticity of vulval development in a rhabditid nematode species. Dev Genes Evol 214:55–63

    Article  PubMed  Google Scholar 

  • Felix MA (2006) Oscheius tipulae. In: Wormbook, The C. elegans Research Community (ed) pp. 1–8

    Google Scholar 

  • Fierst JL, Willis JH, Thomas CG, Wang W, Reynolds RM, Ahearne TE, Cutter AD, Phillips PC (2015) Reproductive mode and the evolution of genome size and structure in Caenorhabditis nematodes. PLoS Genet 11:e1005323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fitch D (2016a) New York University Rhabditid Collection Strains List. 2016 April 20

    Google Scholar 

  • Fitch D (2016b) Worm Systematic Resource Network. 1998 March 29, 1998 April 21

    Google Scholar 

  • Garcia LR, LeBoeuf B, Koo P (2007) Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 175:1761–1771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardner SL, Fong EB, Al Banna L, Raymond SR (1994) A new species of Vexillata (Nemata: Ornithostrongylidae) from the coarse-haired pocket mouse Chaetodipus hispidus in New Mexico. J Parasitol 80:591–594

    Article  CAS  PubMed  Google Scholar 

  • Gerber K, Giblin-Davis RM (1990) Teratorhabditis palmarum n. sp.(Nemata: Rhabditidae): an associate of Rhynchophorus palmarum and R. cruentatus. J Nematol 22(3):337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbons LM, Hoglund J (2002) Dictyocaulus capreolus n. sp. (Nematoda: Trichostrongyloidea) from roe deer, Capreolus capreolus and moose, Alces alces in Sweden. J Helminthol 76(2):119–125

    Article  CAS  PubMed  Google Scholar 

  • Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igic B (2010) Species selection maintains self-incompatibility. Science 330:493–495

    Article  CAS  PubMed  Google Scholar 

  • Gomes D, Pereira da Cruz R, Vicente J, Pinto R (2003) Nematode parasites of marsupials and small rodents from the Brazilian Atlantic Forest in the State of Rio de Janeiro, Brazil. Rev Bras Zool 20(4):699–707

    Article  Google Scholar 

  • Graustein A, Gaspar JM, Walters JR, Palopoli MF (2002) Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161:99–107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grewal P, Grewal S, Malik V, Klein M (2002) Differences in susceptibility of introduced and native white grub species to entomopathogenic nematodes from various geographic localities. Biol Control 24(3):230–237

    Article  Google Scholar 

  • Haag E (2005) The evolution of nematode sex determination:C. elegans as a reference point for comparative biology. In: Wormbook, The C. elegans Research Community (ed)

    Google Scholar 

  • Haag ES (2009) Caenorhabditis nematodes as a model for the adaptive evolution of germ cells. Curr Top Dev Biol 86:43–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa H, Syafruddin (1994) Cyclodontostomum purvisi (Syn. Ancistronema coronatum) (Nematoda: Strongyloidea: Chabertiidae) from rats of Kalimantan and Sulawesi, Indonesia. J Parasitol 80:657–660

    Article  CAS  PubMed  Google Scholar 

  • Hechler HC (1963) Description, developmental biology, and feeding habits of Seinura tenuicaudata (De Man) JB Goodey, 1960 (Nematoda: Aphelenchoididae), a nematode predator. Proc Helminthol Soc Wash 30(2):182–195

    Google Scholar 

  • Hesling J (1966) The effect of some microphagous saprobic nematodes on mushroom culture. Ann Appl Biol 58(3):477–486

    Article  Google Scholar 

  • Hill RC, de Carvalho CE, Salogiannis J, Schlager B, Pilgrim D, Haag ES (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10:531–538

    Article  CAS  PubMed  Google Scholar 

  • Hodgkin J (2002) One lucky XX male: isolation of the first Caenorhabditis elegans sex-determination mutants. Genetics 162:1501–1504

    PubMed  PubMed Central  Google Scholar 

  • Hodgkin JA, Brenner S (1977) Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86:275–287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, Holovachov O, Bakker J, Helder J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown Clades. Mol Biol Evol 23:1792–1800

    Article  CAS  PubMed  Google Scholar 

  • Hooper DJ, Wilson MJ, Rowe JA, Glen DM (1999) Some observations on the morphology and protein profiles of the slug-parasitic nematodes Phasmarhabditis hermaphrodita and P. neopapillosa (Nematoda: Rhabditidae). Nematology 1(2):173–182

    Article  Google Scholar 

  • Huby-Chilton F, Beveridge I, Gasser RB, Chilton NB (2002) Redescription of Zoniolaimus mawsonae Beveridge, 1983 (Nematoda: Strongyloidea) and the description of Z. latebrosus n. sp. from the red kangaroo Macropus rufus (Marsupialia: Macropodidae) based on morphological and molecular data. Syst Parasitol 51(2):135–147

    Article  PubMed  Google Scholar 

  • Jabbar A, Mohandas N, Jex AR, Gasser RB (2013) The mitochondrial genome of Protostrongylus rufescens – implications for population and systematic studies. Parasit Vectors 6(1):263

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanzaki N, Masuya H, Kubono T (2008) Description of Neodiplogaster crenatae sp. n. and N. acaloleptae sp. n.(Nematoda: Diplogastridae) from Japan. Nematology 10(4):545–560

    Article  Google Scholar 

  • Kanzaki N, Giblin-Davis RM, Wcislo WT, Zeng Y, Ye W, Center BJ, Esquivel A, Thomas KW (2010) Acrostichus megaloptae n. sp.(Nematoda: Diplogastridae), a phoretic associate of Megalopta spp.(Hymenoptera: Halictidae) in Central America. Nematology 12(3):453–468

    Article  Google Scholar 

  • Kanzaki N, Taki H, Masuya H, Okabe K, Tanaka R, Abe F (2011) Diversity of stag beetle-associated nematodes in Japan. Environ Entomol 40(2):281–288

    Article  Google Scholar 

  • Kanzaki N, Ragsdale EJ, Herrmann M, Mayer WE, Sommer RJ (2012) Description of three Pristionchus species (Nematoda: Diplogastridae) from Japan that form a cryptic species complex with the model organism P. pacificus. Zool Sci 29:403–417

    Article  Google Scholar 

  • Kanzaki N, Ragsdale EJ, Herrmann M, Susoy V, Sommer RJ (2013) Two androdioecious and one dioecious new species of Pristionchus (Nematoda: Diplogastridae): new reference points for the evolution of reproductive mode. J Nematol 45:172–194

    PubMed  PubMed Central  Google Scholar 

  • Kanzaki N, Ragsdale EJ, Giblin-Davis RM (2014) Revision of the paraphyletic genus Koerneria Meyl, 1960 and resurrection of two other genera of Diplogastridae (Nematoda). Zookeys 442:17–30

    Article  Google Scholar 

  • Kanzaki N, Kiontke K, Tanaka R, Hirooka Y, Schwarz A, Muller-Reichert T, Chaudhuri J, Pires-daSilva A (2017) Description of two three-gendered nematode species in the new genus Auanema (Rhabditina) that are models for reproductive mode evolution. Sci Rep 7:11135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kavetska KM, Krolaczyk K, Stapf A, Grzesiak W, Kalisinska E, Pilarczyk B (2011) Revision of the species complex Amidostomum acutum (Lundahl, 1848) (Nematoda: Amidostomatidae). Parasitol Res 109(1):105–117

    Article  PubMed  PubMed Central  Google Scholar 

  • Kelleher DF, de Carvalho CE, Doty AV, Layton M, Cheng AT, Mathies LD, Pilgrim D, Haag ES (2008) Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae. Genetics 178:1415–1429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimble J, Crittenden SL (2007) Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 23:405–433

    Article  CAS  PubMed  Google Scholar 

  • Kiontke K, Fitch DH (2005) The phylogenetic relationships of Caenorhabditis and other rhabditids. WormBook. Aug 11:1–11

    Google Scholar 

  • Kiontke K, Manegold A, Sudhaus W (2001) Redescription of Diplogasteroides nasuensis Takaki, 1941 and D. magnus Völk, 1950 (Nematoda: Diplogastrina) associated with Scarabaeidae (Coleoptera). Nematology 3(8):817–832

    Article  Google Scholar 

  • Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101:9003–9008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiontke KC, Felix MA, Ailion M, Rockman MV, Braendle C, Penigault JB, Fitch DH (2011) A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11:339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ko R, Anderson R (1972) Tissue migration, growth, and morphogenesis of Filaroides martis (Nematoda: Metastrongyloidea) in mink (Mustela vison). Can J Zool 50(12):1637–1649

    Article  CAS  PubMed  Google Scholar 

  • Kontrimavichus VL, Deliamure SL, Boev SN (1985) Metastrongyloids of domestic and wild animals. Academy of Sciences of the USSR Helminthological Institute Fundamentals of Nematology 1985: U.S. Department of Agriculture and the National Science Foundation

    Google Scholar 

  • Korner H (1954) The nematode fauna of rotting wood and their relationship with insects. Zoologische Jahrbücher. Abteilung fur Systematik, Ökologie und Geographie der Tiere 82(3/4):245–353

    Google Scholar 

  • Krone O, Friedrich D, Honisch M (2007) Specific status and pathogenicity of syngamid nematodes in bird species (Ciconiformes, Falconiformes, Gruiformes) from Germany. J Helminthol 81(1):67–73

    Article  CAS  PubMed  Google Scholar 

  • Kuchboev AE, Krucken J, Ruziev BH, von Samson-Himmelstjerna G (2015) Molecular phylogeny and diagnosis of species of the family Protostrongylidae from caprine hosts in Uzbekistan. Parasitol Res 114(4):1355–1364

    Article  PubMed  Google Scholar 

  • Kuwabara PE (1996) Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2. Genetics 144:597–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lahl V, Sadler B, Schierenberg E (2006) Egg development in parthenogenetic nematodes: variations in meiosis and axis formation. Int J Dev Biol 50(4):393

    Article  PubMed  Google Scholar 

  • Langford GJ, Janovy J Jr (2009) Comparative life cycles and life histories of North American Rhabdias spp. (Nematoda: Rhabdiasidae): lungworms from snakes and anurans. J Parasitol 95:1145–1155

    Article  PubMed  Google Scholar 

  • Lehnert K, von Samson-Himmelstjerna G, Schaudien D, Bleidorn C, Wohlsein P, Siebert U (2010) Transmission of lungworms of harbour porpoises and harbour seals: molecular tools determine potential vertebrate intermediate hosts. Int J Parasitol 40(7):845–853

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Haag ES (2014) Evolutionarily dynamic roles of a PUF RNA-binding protein in the somatic development of Caenorhabditis briggsae. J Exp Zool B Mol Dev Evol 322:129–141

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Stumpf C, Wickens M, Haag ES (2012) Context-dependent function of a conserved translational regulatory module. Development 139:1509–1521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    Article  CAS  PubMed  Google Scholar 

  • Mackerras M, Sandars D (1955) The life history of the rat lung-worm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Australian J Zool 3(1):1–21

    Article  Google Scholar 

  • Maddison W, Maddison D (2015) Mesquite: a modular system for evolutionary analysis, Version 3.04 ed

    Google Scholar 

  • Maddison WP, Midford PE, Otto SP (2007) Estimating a binary character’s effect on speciation and extinction. Syst Biol 56:701–710

    Article  PubMed  Google Scholar 

  • Mawson PM (1960) Two new species of trichostrongyle nematodes from the Australian pouched mouse, Phascogale flavipes (Waterhouse). Parasitology 50(3–4):425–429

    Article  CAS  Google Scholar 

  • Mawson PM (1964) Some Nematoda (Strongylina and Oxyurina) from kangaroos (Macropus spp.) from eastern Australia. Parasitology 54(02):237–262

    Article  CAS  PubMed  Google Scholar 

  • Mayer WE, Herrmann M, Sommer RJ (2007) Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism. BMC Evol Biol 7:104

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer WE, Herrmann M, Sommer RJ (2009) Molecular phylogeny of beetle associated diplogastrid nematodes suggests host switching rather than nematode-beetle coevolution. BMC Evol Biol 9:212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monet-Mendoza A, Osorio-Sarabia D, Garcia-Prieto L (2005) Helminths of the Virginia opossum Didelphis virginiana (Mammalia: Didelphidae) in Mexico. J Parasitol 91(1):213–219

    Article  PubMed  Google Scholar 

  • Morand S (1992) Angiostoma spiridonovi n. sp.(Nematoda: Angiostomatidae) from Limax flavus (Gastropoda: Limacidae). J Helminthol Soc Wash 59(2):212–217

    Google Scholar 

  • Morand S, Barker GM (1995) Angiostoma schizoglossae n. sp. (Nematoda: Angiostomatidae) from the New Zealand endemic slug Schizoglossa novoseelandica (Gastropoda: Rhytididae). J Parasitol 81(1):94–98

    Article  CAS  PubMed  Google Scholar 

  • Morera P (1973) Life history and redescription of Angiostrongylus costaricensis Morera and Cespedes, 1971. Am J Trop Med Hyg 22(5):613–621

    Article  CAS  PubMed  Google Scholar 

  • Morita T, Haruta K, Shibata-Haruta A, Kanda E, Imai S, Ike K (2007) Lung worms of wild boars in the western region of Tokyo, Japan. J Vet Med Sci 69(4):417–420

    Article  PubMed  Google Scholar 

  • Morran LT, Parmenter MD, Phillips PC (2009) Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462:350–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morran LT, Schmidt OG, Gelarden IA, Parrish RC 2nd, Lively CM (2011) Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333:216–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moser M, Rhinehart H (1993) The lungworm, Halocercus spp. (Nematoda: Pseudaliidae) in cetaceans from California. J Wildl Dis 29(3):507–508

    Article  CAS  PubMed  Google Scholar 

  • Nasrallah JB, Nasrallah ME (2014) S-locus receptor kinase signalling. Biochem Soc Trans 42:313–319

    Article  CAS  PubMed  Google Scholar 

  • Nayak S, Goree J, Schedl T (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3:e6

    Article  CAS  PubMed  Google Scholar 

  • Nematology Lab at University of Nebraska (2016) L plant and insect parasitic nematodes. http://nematode.unl.edu/bunosp.htm

  • Nemetschke L, Eberhardt AG, Hertzberg H, Streit A (2010) Genetics, chromatin diminution, and sex chromosome evolution in the parasitic nematode genus Strongyloides. Curr Biol 20:1687–1696

    Article  CAS  PubMed  Google Scholar 

  • Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, Aduna A, Laurita J, Kruglyak L (2008) Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454:1019–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pillai J, Taylor D (1968) Emendation of the Genus Demaniella Steiner, 1914 (Nematoda: Diplogasterinae), with observations on the biology of D. Basili N. Sp. Nematologica 14(2):285–294

    Article  Google Scholar 

  • Poinar G, Jackson T, Klein M (1987) Heterorhabditis megidis sp. n. (Heterorhabditidae: Rhabditida), parasitic in the Japanese beetle, Popillia japonica (Scarabaeidae: Coleoptera), in Ohio. Proc Helminthol Soc Wash 54:53–59

    Google Scholar 

  • Powers T (2016, April 20) Plant and insect parasitic nematodes. http://nematode.unl.edu/

  • Reynolds LA, Filbey KJ, Maizels RM (2012) Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin Immunopathol 34(6):829–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribas A, Casanova JC (2002) Agfa morandi sp. n. (Rhabditida, Agfidae) a parasite of Limax sp. (Gastropoda, Limacidae). Parasitol Res 88(8):745–747

    Article  CAS  PubMed  Google Scholar 

  • Romanowski RD (1982) Purification and properties of a ribonuclease from the excretory gland cells of Stephanurus dentatus. Mol Biochem Parasitol 5(2):77–92

    Article  CAS  PubMed  Google Scholar 

  • Saari SA, Nikander SE (2006) Pelodera (syn. Rhabditis) strongyloides as a cause of dermatitis–a report of 11 dogs from Finland. Acta Vet Scand 48(1):18

    Article  PubMed  PubMed Central  Google Scholar 

  • Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119:43–61

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider B, Jariwala AR, Periago MV, Gazzinelli MF, Bose SN, Hotez PJ, Diemert DJ, Bethony JM (2011) A history of hookworm vaccine development. Hum Vaccin 7(11):1234–1244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulte F (1989) Description of Rhabditis (Pelodera) pseudoteres n. sp.(Rhabditidae: Nematoda) with a redescription of its sibling R.(P.) teres (Schneider, 1866). Revue Nématol 12(4):387–394

    Google Scholar 

  • Schurko AM, Neiman M, Logsdon JM Jr (2009) Signs of sex: what we know and how we know it. Trends Ecol Evol 24:208–217

    Article  PubMed  Google Scholar 

  • Sharifiyazdi H, Moghaddar N, Delavari I, Gorjipoor S (2015) Genetic characterization of Nematodirella cameli based on 18S rDNA and cytochrome c oxidase subunit 1 (CO1). J Fac Vet Med Istanbul Univ 41(1):50–59

    Google Scholar 

  • Sicard A, Lenhard M (2011) The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann Bot 107:1433–1443

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva AV, Costa HM, Santos HA, Carvalho RO (1999) Cyathostominae (Nematoda) parasites of Equus caballus in some Brazilian states. Vet Parasitol 86(1):15–21

    Article  CAS  PubMed  Google Scholar 

  • Spieler M, Schierenberg E (1995) On the development of the alternating free-living and parasitic generations of the nematode Rhabdias bufonis. Invert Reprod Dev 28:193–203

    Article  Google Scholar 

  • Spratt DM (2015) Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. Int J Parasitol Parasites Wildl 4(2):178–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Stock S, Hunt D (2005) Morphology and systematics of nematodes used in biocontrol. In: Grewal P, Ehlers R-U, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI, Oxfordshire, UK

    Google Scholar 

  • Stock SP, Strong DR, Gardner SL (1996) Identification of Heterorhabditis (Nematoda: Heterorhabditidae) from California with a new species isolated from the larvae of the ghost moth Hepialis californicus (Lepidoptera: Hepialidae) from the Bodega Bay Natural Reserve. Fundam Appl Nematol 19(6):585–592

    Google Scholar 

  • Stock SP, Caicedo AM, Calatayud PA (2005) Rhabditis (Oscheius) colombiana n. sp.(Nematoda: Rhabditidae), a necromenic associate of the subterranean burrower bug Cyrtomenus bergi (Hemiptera: Cydnidae) from the Cauca Valley, Colombia. Nematology 7(3):363–373

    Article  Google Scholar 

  • Strauch O, Stoessel S, Ehlers R-U (1994) Culture conditions define automictic or amphimictic reproduction in entomopathogenic rhabditid nematodes of the genus Heterorhabditis. Fundam Appl Nematol 17(6):575–582

    Google Scholar 

  • Streit A, Li W, Robertson B, Schein J, Kamal I, Marra M, Wood W (1999) Homologs of the Caenorhabditis elegans masculinizing gene her-1 in C. briggsae and the filarial parasite Brugia malayi. Genetics 152:1573–1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suarez V, Cabaret J (1992) Interbreeding in the subfamily Ostertagiinae (Nematoda: Trichostrongylidae) of ruminants. J Parasitol 78:402–405

    Article  CAS  PubMed  Google Scholar 

  • Sudhaus W (1978) Systematik, Phylogenie und Okologie der holzbewohnenden Nematoden Gruppe Rhabditis (Mesorhabditis) und das Problem “geschlechtsbezogener” Artdifferenzierung. Veb G. Fischer Verlag, Jena

    Google Scholar 

  • Sudhaus W (1993) Redescription of Rhabditis (Oscheius) tipulae (Nematoda: Rhabditidae) associated with leatherjackets, larvae of Tipula paludosa (Diptera: Tipulidae). Nematologica 39(1):234–239

    Article  Google Scholar 

  • Sudhaus W, Fitch D (2001) Comparative studies on the phylogeny and systematics of the rhabditidae (nematoda). J Nematol 33(1):1–70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor M, Hunt K, Smith G, Otter A (2000) Deletrocephalus dimidiatus in greater rheas (Rhea americana) in the UK. Vet Rec 146(1):19–20

    Article  CAS  PubMed  Google Scholar 

  • Thomas CG, Li R, Smith HE, Woodruff GC, Oliver B, Haag ES (2012a) Simplification and desexualization of gene expression in self-fertile nematodes. Curr Biol 22:2167–2172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas CG, Woodruff GC, Haag ES (2012b) Causes and consequences of the evolution of reproductive mode in Caenorhabditis nematodes. Trends Genet 28:213–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ting JJ, Woodruff GC, Leung G, Shin N-R, Cutter AD, Haag ES (2014) Intense sperm-mediated sexual conflict promotes reproductive isolation in Caenorhabditis nematodes. PLoS Biol 12:e1001915

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tomalak M, Welch HE, Galloway TD (1989) Parasitism of Parasitorhabditis obtusa and P. autographi (Nematoda: Rhabditidae) in the digestive tract of their bark beetle (Coleoptera: Scolytidae) hosts. J Invertebr Pathol 53(1):57–63

    Article  Google Scholar 

  • Umair S, McMurtry LW, Knight JS, Simpson HV (2016) Use of fluorescent lectin binding to distinguish eggs of gastrointestinal nematode parasites of sheep. Vet Parasitol 217:76–80

    Article  CAS  PubMed  Google Scholar 

  • Urquhart G, Armour J, Duncan J, Jennings F, Dunn A (1996) Veterinary parisitology, 2nd edn. Longman, Harlow, UK

    Google Scholar 

  • Vacquier VD, Swanson WJ (2011) Selection in the rapid evolution of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol 3:a002931

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Gansbeke R, Bert W, Govaerts A, Claeys M, Van Driessche R, Manhout J, Borgonie G (2004) Cuticular structure of three Bunonema species and first description of the male of B. penardi Stefanski, 1914 (Nematoda: Bunonematidae). Nematology 6:473–484

    Article  Google Scholar 

  • van Megen H, den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T, Holovachov O, Bakker J, Helder J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950

    Article  CAS  Google Scholar 

  • Varcasia A, Brianti E, Tamponi C, Pipia AP, Cabras PA, Mereu M, Dantas-Torres F, Scala A, Otranto D (2015) Simultaneous infection by four feline lungworm species and implications for the diagnosis. Parasitol Res 114(1):317–321

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Chen PJ, Wang GJ, Keller L (2010) Chromosome size differences may affect meiosis and genome size. Science 329:293

    Article  CAS  PubMed  Google Scholar 

  • Wei Q, Zhao Y, Guo Y, Stomel J, Stires R, Ellis RE (2014) Co-option of alternate sperm activation programs in the evolution of self-fertile nematodes. Nat Commun 5:5888

    Article  CAS  PubMed  Google Scholar 

  • Wright SI, Kalisz S, Slotte T (2013) Evolutionary consequences of self-fertilization in plants. Proc Biol Sci 280:20130133

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, De Ley P, Liang Y (2001) Description of a new species of the Genus Tylopharynx (Nemata: Diplogasteroidea), T. clariamphida sp. n., with a redescription of T. foetida (Bütschli, 1874) Goffart, 1930. J Nematol 33(2–3):83

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JC, Go AC, Samson M, Cintra T, Mirsoian S, Wu TF, Jow MM, Routman EJ, Chu DS (2012) Sperm development and motility are regulated by PP1 phosphatases in Caenorhabditis elegans. Genetics 190:143–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin D, Schwarz EM, Thomas CG, Felde RL, Korf IF, Cutter AD, Schartner CM, Ralston EJ, Meyer BJ, Haag ES (2018) Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins. Science 359:55–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young KA, Liu Y, Wang Z (2008) The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp Biochem Physiol C Toxicol Pharmacol 148:401–410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zarkower D (2006) Somatic sex determination (Feb. 10, 2006). In: Wormbook, The C. elegans Research Community (ed), pp 1–12

    Google Scholar 

  • Zhang C, Liu J, Xu M, Sun J, Yang S, An X, Gao G, Lin M, Lai R, He Z, Wu Y, Zhang K (2008) Heterorhabditidoides chongmingensis gen. nov., sp. nov. (Rhabditida: Rhabditidae), a novel member of the entomopathogenic nematodes. J Invertebr Pathol 98(2):153–168

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Drs. Lynn Carta, David Fitch, Augustin Jimenez, Natsumi Kanzaki, and Karin Kiontke for helping in determining the reproductive mode of some species, Dr. Erich Schwartz for sharing unpublished genome assembly sizes, Dr. Arlin Stoltzfus for useful discussions, and Ralf Sommer for use of an image. Research described in this chapter was supported by NIH grant GM079414 and NSF grant IOS-1355119, both to ESH.

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Authors and Affiliations

  1. Department of Biology, University of Maryland, College Park, MD, USA

    Eric S. Haag, Da Yin & Shuang Hu

  2. Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands

    Johannes Helder & Paul J. W. Mooijman

Authors
  1. Eric S. Haag
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  2. Johannes Helder
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  3. Paul J. W. Mooijman
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  4. Da Yin
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  5. Shuang Hu
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Correspondence to Eric S. Haag .

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  1. Joseph M. Long Marine Laboratory, Institute of Marine Sciences, University of California, Santa Cruz, CA, USA

    Janet L. Leonard

Appendix: Sources for Sexual Modes in Fig. 4.2

Appendix: Sources for Sexual Modes in Fig. 4.2

Species

References

Angiostrongylus

costaricensis

Spratt (2015), Morera (1973)

Angiostrongylus

dujardini

Spratt (2015), Drozdz et al. (1971), Eira et al. (2006)

Angiostrongylus

vasorum

Spratt (2015), Costa et al. (2003)

Angiostrongylus

malaysiensis

Spratt (2015), Bhaibulaya and Cross (1971)

Angiostrongylus

cantonensis

Spratt (2015), Mackerras and Sandars (1955)

Parafilaroides

decorus

Dailey (2009)

Halocercus

invaginatus

Moser and Rhinehart (1993)

Stenurus

minor

Faulkner et al. (1998)

Torynurus

convolutus

Baylis and Daubney (1925)

Filaroides

martis

Ko and Anderson (1972)

Metastrongylus

elongates/salmi

Morita et al. (2007)

Oslerus

rostratus

Varcasia et al. (2015), Bowman et al. (2002)

Oslerus

osleri

Varcasia et al. (2015), Bowman et al. (2002)

Dictyocaulus

eckerti

Divina et al. (2000)

Dictyocaulus

capreolus

Gibbons and Hoglund (2002)

Dictyocaulus

viviparus

Divina et al. (2000)

Dictyocaulus

filaria

Urquhart et al. (1996)

Protostrongylus

rufescens

Jabbar et al. (2013)

Muellerius

capillaris

Kuchboev et al. (2015)

Aelurostrongylus

abstrusus

Urquhart et al. (1996)

Parelaphostrongylus

odocoilei

Kontrimavichus et al. (1985)

Skrjabingylus

chitwoodorum

Kontrimavichus et al. (1985)

Otostrongylus

circumlitus

Lehnert et al. (2010)

Crenosoma

vulpis

Kontrimavichus et al. (1985)

Crenosoma

striatum

Kontrimavichus et al. (1985)

Crenosoma

mephitidis

Kontrimavichus et al. (1985)

Troglostrongylus

wilsoni

Kontrimavichus et al. (1985)

Viannaia

viannai

Monet-Mendoza et al. (2005)

Viannaia

hamata

Gomes et al. (2003)

Herpetostrongylus

pythonis

Durett-Desset (2009)

Austrostrongylus

victoriensis

Beveridge and Durett-Desset (1986)

Nicollina

cameroni

Durette-Desset and Cassone (1983)

Travassostrongylus

callis

Cameron and Myers (1961)

Travassostrongylus

orloffi

Cameron and Myers (1961)

Heligmosomoides

polygyrus

Reynolds et al. (2012)

Nippostrongylus

brasiliensis

Camberis et al. (2003)

Vexillata

convoluta

Gardner et al. (1994)

Deletrocephalus

dimidiatus

Taylor et al. (2000)

Ancylostoma

duodenale

Schneider et al. (2011)

Ancylostoma

caninum

Schneider et al. (2011)

Hovorkonema

variegatum

Krone et al. (2007)

Syngamus

trachea

Urquhart et al. (1996)

Necator

americanus

Schneider et al. (2011)

Cyclodontostomum

purvisi

Hasegawa and Syafruddin (1994)

Chabertia

ovina

Umair et al. (2016)

Zoniolaimus

mawsonae

Huby-Chilton et al. (2002)

Hypodontus

macropi

Beveridge (1979)

Labiostrongylus

bipapillosus

Chilton et al. (2003)

Stephanurus

dentatus

Romanowski (1982)

Strongylus

equinus

Urquhart et al. (1996)

Petrovinema

poculatum

Silva et al. (1999)

Kalicephalus

cristatus

Chilton et al. (2006)

Trichostrongylus

colubriformis

Urquhart et al. (1996)

Ostertagia

ostertagi

Urquhart et al. (1996)

Ostertagia

leptospicularis

Suarez and Cabaret (1992)

Nematodirus

battus

Urquhart et al. (1996)

Nematodirella

cameli

Sharifiyazdi et al. (2015)

Filarinema

flagrifer

Mawson (1964)

Tetrabothriostrongylus

mackerrasae

Mawson (1960)

Amidostomum

cygni

Kavetska et al. (2011)

Haemonchus

contortus

Urquhart et al. (1996)

Heterorhabditis

megidis

Ehlers et al. (1998)

Heterorhabditis

bacteriophora

Ciche (2007)

Heterorhabditis

hepialus

Stock et al. (1996)

Heterorhabditis

sp. 1

Strauch et al. (1994)

Heterorhabditis

zealandica

Grewal et al. (2002)

Rhabditis

colombiana

Stock et al. (2005)

Oscheius

sp. 3

Felix (2006)

Oscheius

insectivora

Felix (2006)

Oscheius

myriophila

Felix (2006)

Heterorhabditoides

chongmingensis

Zhang et al. (2008)

Heterorhabditidoides

sp. 1

Felix (2006)

Oscheius

dolichura

Felix (2006)

Oscheius

sp. 1

Felix (2006)

Oscheius

dolichuroides

Felix (2006)

Oscheius

guentheri

Felix (2006)

Oscheius

tipulae

Sudhaus (1993)

Pellioditis

mediterranea

Fitch (2016a)

Pellioditis

marina

Andrássy (1983)

Cephaloboides

nidrosiensis

Fitch (2016a)

Cephaloboides

cf. armata

Sudhaus and Fitch (2001)

Curviditis

sp. 1

 

Rhabditella

sp. 1

 

Rhabditella

axei

Fitch (2016a)

Agfa

flexilis

Ribas and Casanova (2002)

Phasmarhabditis

hermaphrodita

Stock and Hunt (2005)

Phasmarhabditis

sp. 1 (neopapillosa)

Hooper et al. (1999)

Angiostoma

dentifera

Morand (1992), Morand and Barker (1995)

Angiostoma

limacis

Morand (1992), Morand and Barker (1995)

Pellioditis

typica

Kiontke and Fitch (2005)

Rhabditis

blumi

Kiontke and Fitch (2005)

Rhabditis

rainai

Carta and Osbrink (2005)

Cruznema

sp. 1

L. Carta (personal communication)

Cruznema

tripartitum

L. Carta (personal communication)

Caenorhabditis

briggsae

Kiontke et al. (2011)

Caenorhabditis

remanei

Kiontke et al. (2011)

Caenorhabditis

japonica

Kiontke et al. (2011)

Caenorhabditis

sp. 2

Kiontke et al. (2011)

Caenorhabditis

elegans

Kiontke et al. (2011)

Caenorhabditis

sinica

Kiontke et al. (2011)

Caenorhabditis

sp. 1

Kiontke et al. (2011)

Caenorhabditis

plicata

Kiontke et al. (2011)

Caenorhabditis

drosophilae

Kiontke et al. (2011)

Caenorhabditis

brenneri

Kiontke et al. (2011)

Caenorhabditis

angaria

Kiontke et al. (2011)

Caenorhabditis

sonorae

Kiontke et al. (2011)

Diploscapter

coronatus

Lahl et al. (2006)

Protorhabditis

sp. 3

Kiontke and Fitch (2005)

Protorhabditis

sp. 2

Fitch (2016b)

Prodontorhabditis

wirthi

Fitch (2016a)

Protorhabditis

sp. 1

Fitch (2016a)

Choriorhabditis

cristata

Kiontke and Fitch (2005)

Choriorhabditis

dudichi

Fitch (2016a)

Mesorhabditis

sp. 2

L. Carta (personal communication)

Mesorhabditis

sp. 1

L. Carta (personal communication)

Mesorhabditis

sp. 2

L. Carta (personal communication)

Mesorhabditis

sp. 3

L. Carta (personal communication)

Mesorhabditis

sp. 4

L. Carta (personal communication)

Mesorhabditis

sp. 2G

L. Carta (personal communication)

Mesorhabditis

sp. 3G

L. Carta (personal communication)

Mesorhabditis

longespiculosa

Fitch (2016a)

Mesorhabditis

anisomorpha

Sudhaus (1978)

Mesorhabditis

miotki

Sudhaus (1978)

Parasitorhabditis

sp. 1

Tomalak et al. (1989)

Parasitorhabditis

obtusa

Tomalak et al. (1989)

Mesorhabditis

scanica

L. Carta (personal communication)

Teratorhabditis

synpapillata

Fitch (2016a)

Teratorhabditis

palmarum

Gerber and Giblin-Davis (1990)

Teratorhabditis

stiannula

Fitch (2016a)

Teratorhabditis

mariannae

Fitch (2016a)

Pelodera

pseudoteres

Schulte (1989)

Pelodera

teres

Schulte (1989)

Pelodera

punctata

Fitch (2016a)

Pelodera

strongyloides

Saari and Nikander (2006)

Pelodera

cylindrica

Hesling (1966)

Rhabditoides

regina

Fitch (2016a)

Rhabditoides

inermis

Kiontke and Fitch (2005)

Rhabditidoides

sp. 1

Fitch (2016a)

Diplogasteroides

magnus

Kiontke et al. (2001)

Diplogasteroides

sp. 2

M. Hermann (personal communication)

Diplogastrellus

sp. 3

Fitch (2016a)

Pseudodiplogasteroides

compositus

Korner (1954)

Diplogastrellus

sp. 1

Fitch (2016a)

Rhabditolaimus

leuckarti

V. Susoy (personal communication)

Myctolaimus

sp. 1

P. De Ley (personal communication)

Myctolaimus

sp. 2

P. De Ley (personal communication)

Pristionchus

(all species)

Mayer et al. (2007)

Oigolaimella

sp. 2

N. Kanzaki (personal communication)

Demaniella

sp. 1

Pillai and Taylor (1968)

Oigolaimella

sp. 1

N. Kanzaki (personal communication)

Fictor

sp. 1

Powers (2016)

Acrostichus

sp. 1

Kanzaki et al. (2010)

Acrostichus

sp. 5

Kanzaki et al. (2010)

Acrostichus

halicti

Kiontke and Fitch (2005)

Diplogaster

rivalis

Abolafia (2006)

Mononchoides

striatus

Calaway and Tarjan (1973)

Neodiplogaster

sp. 1

Kanzaki et al. (2008)

Tylopharynx

foetida

Wu et al. (2001)

Koerneria

sp. 1

Mayer et al. (2007)

Koerneria

lucani

Kanzaki et al. (2014)

Diplenteron

colobocercus

Bongers et al. (1988)

Koerneria

luziae

Kanzaki et al. (2011)

Bunonema

reticulatum a

Holterman and Helder (unpublished observations), Fitch (2016a)

Bunonema

richtersi a

Van Gansbeke et al. (2004), Nematology Lab at University of Nebraska (2016)

Rhabditoides

inermiformis

Kiontke and Fitch (2005)

Poikilolaimus

sp. 4

N. Kanzaki (personal communication)

Poikilolaimus

sp. 3

N. Kanzaki (personal communication)

Poikilolaimus

sp. 5

N. Kanzaki (personal communication)

Poikilolaimus

sp. 1

N. Kanzaki (personal communication)

Poikilolaimus

oxycercus

Fitch (2016a), Kiontke and Fitch (2005)

Seinura

tenuicaudata

Hechler (1963)

Odontopharynx

longicaudata

Chitambar and Noffsinger (1989)

Myolaimus

sp. 1

Cobb (1920)

  1. aThough reproduction of this strain is uniparental, it is not clear whether it is via parthenogenesis or selfing

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Haag, E.S., Helder, J., Mooijman, P.J.W., Yin, D., Hu, S. (2018). The Evolution of Uniparental Reproduction in Rhabditina Nematodes: Phylogenetic Patterns, Developmental Causes, and Surprising Consequences. In: Leonard, J. (eds) Transitions Between Sexual Systems. Springer, Cham. https://doi.org/10.1007/978-3-319-94139-4_4

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