Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-17T18:28:31.192Z Has data issue: false hasContentIssue false

How to become a parasite without sex chromosomes: a hypothesis for the evolution of Strongyloides spp. and related nematodes

Published online by Cambridge University Press:  14 May 2014

ADRIAN STREIT*
Affiliation:
Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, Spemannstrasse 35, D-72076 Tübingen, Germany
*
*Corresponding author: Max-Planck-Institut für Entwicklungsbiologie, Abteilung IV, Evolutionsbiologie, Spemannstrasse 35, D-72076 Tübingen, Germany. E-mail: adrian.streit@tuebingen.mpg.de

Summary

Parasitic lifestyles evolved many times independently. Just within the phylum Nematoda animal parasitism must have arisen at least four times. Switching to a parasitic lifestyle is expected to lead to changes in various life history traits including reproductive strategies. Parasitic nematode worms of the genus Strongyloides represent an interesting example to study these processes because they are still capable of forming facultative free-living generations in between parasitic ones. The parasitic generation consists of females only, which reproduce parthenogenetically. The sex in the progeny of the parasitic worms is determined by environmental cues, which control a, presumably ancestral, XX/XO chromosomal sex determining system. In some species the X chromosome is fused with an autosome and one copy of the X-derived sequences is removed by sex-specific chromatin diminution in males. Here I propose a hypothesis for how today's Strongyloides sp. might have evolved from a sexual free-living ancestor through dauer larvae forming free-living and facultative parasitic intermediate stages.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albertson, D. G., Nwaorgu, O. C. and Sulston, J. E. (1979). Chromatin diminution and a chromosomal mechanism of sexual differentiation in Strongyloides papillosus . Chromosoma 75, 7587.Google Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Augustine, D. L. (1940). Experimental studies on the validity of species in the genus Strongyloides . American Journal of Hygiene 32, 2432.Google Scholar
Baldi, C., Cho, S. and Ellis, R. E. (2009). Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326, 10021005.Google Scholar
Beach, T. D. (1936). Experimental studies on human and primate species of Strongyloides – V. The free-living phase of the life cycle. American Journal of Hygiene 23, 243277.Google Scholar
Beg, M. K. (1968). Studies on the life-cycle of Strongyloides fulleborni von Linstow, 1905. Annals of Tropical Medicine and Parasitology 62, 502505.Google Scholar
Blaxter, M., Koutsovoulos, G., Jones, M., Kumar, S. and Elsworth, B. (2014). Phylogenomics of nematoda. In Systematics Association Special Volume on Next Generation Systematics (ed. Cotton, J., Hughes, J. and Olsen, P.). Cambridge University Press, Cambridge, UK.Google Scholar
Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.Google Scholar
Brenner, S. (1974). The genetics of Caenorhabditis elegans . Genetics 77, 7194.Google Scholar
Chandler, C. H., Phillips, P. C. and Janzen, F. J. (2009). The evolution of sex-determining mechanisms: lessons from temperature-sensitive mutations in sex determination genes in Caenorhabditis elegans . Journal of Evolutionary Biology 22, 192200.Google Scholar
Chapman, T., Arnquist, G., Bangham, J. and Rowe, L. (2003). Sexual conflict. Trends in Ecology and Evolution 18, 4147.Google Scholar
Crook, M. (2014). The dauer hypothesis and the evolution of parasitism: 20 years on and still going strong. International Journal for Parasitology 44, 18. doi: 10.1016/j.ijpara.2013.08.004.Google Scholar
Denver, D. R., Clark, K. A. and Raboin, M. J. (2011). Reproductive mode evolution in nematodes: insights from molecular phylogenies and recently discovered species. Molecular Phylogenetics and Evolution 61, 584592.Google Scholar
Dieterich, C. and Sommer, R. J. (2009). How to become a parasite – lessons from the genomes of nematodes. Trends in Genetics 25, 203209.Google Scholar
Dorris, M., Viney, M. E. and Blaxter, M. L. (2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32, 15071517.CrossRefGoogle ScholarPubMed
Dubendorfer, A., Hediger, M., Burghardt, G. and Bopp, D. (2002). Musca domestica, a window on the evolution of sex-determining mechanisms in insects. International Journal of Developmental Biology 46, 7579.Google Scholar
Eberhardt, A. G., Mayer, W. E. and Streit, A. (2007). The free-living generation of the nematode Strongyloides papillosus undergoes sexual reproduction. International Journal for Parasitology 37, 9891000.Google Scholar
Eberhardt, A. G., Mayer, W. E., Bonfoh, B. and Streit, A. (2008). The Strongyloides (Nematoda) of sheep and the predominant Strongyloides of cattle form at least two different, genetically isolated populations. Veterinary Parasitology, 157, 8999. doi: 10.1016/j.vetpar.2008.07.019.Google Scholar
Engelstadter, J. (2008). Constraints on the evolution of asexual reproduction. Bioessays, 30, 11381150.Google Scholar
Ferrari, F., Alekseyenko, A. A., Park, P. J. and Kuroda, M. I. (2014). Transcriptional control of a whole chromosome: emerging models for dosage compensation. Nature Structural and Molecular Biology 21, 118125. doi: 10.1038/nsmb.2763.Google Scholar
Grant, W. N., Skinner, S. J., Howes, J. N., Grant, K., Shuttleworth, G., Heath, D. D. and Shoemaker, C. B. (2006 a). Heritable transgenesis of Parastrongyloides trichosuri: a nematode parasite of mammals. International Journal for Parasitology 36, 475483.Google Scholar
Grant, W. N., Stasiuk, S., Newton-Howes, J., Ralston, M., Bisset, S. A., Heath, D. D. and Shoemaker, C. B. (2006 b). Parastrongyloides trichosuri, a nematode parasite of mammals that is uniquely suited to genetic analysis. International Journal for Parasitology, 36, 453466.Google Scholar
Haag, E. S. (2007). Why two sexes? Sex determination in multicellular organisms and protistan mating types. Seminars in Cell and Developmental Biology 18, 348349.Google Scholar
Haag, E. S. and Doty, A. V. (2005). Sex determination across evolution: connecting the dots. PLoS Biology 3, e21.Google Scholar
Hamilton, W. D. (1967). Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156, 477488.Google Scholar
Hammond, M. P. and Robinson, R. D. (1994). Chromosome complement, gametogenesis, and development of Strongyloides stercoralis . Journal of Parasitology 80, 689695.Google Scholar
Hansen, E. L., Buecher, E. J. and Cryan, W. S. (1969). Strongyloides fulleborni: environmental factors and free-living generations. Experimental Parasitology 26, 336343.Google Scholar
Harvey, S. C. and Viney, M. E. (2001). Sex determination in the parasitic nematode Strongyloides ratti . Genetics 158, 15271533.Google Scholar
Hasegawa, H., Hayashida, S., Ikeda, Y. and Sato, H. (2009). Hyper-variable regions in 18S rDNA of Strongyloides spp. as markers for species-specific diagnosis. Parasitology Research 104, 869874.Google Scholar
Hediger, M., Henggeler, C., Meier, N., Perez, R., Saccone, G. and Bopp, D. (2010). Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184, 155170.Google Scholar
Herrmann, M., Mayer, W. E. and Sommer, R. J. (2006). Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in Western Europe. Zoology (Jena) 109, 96108.Google Scholar
Herrmann, M., Kienle, S., Rochat, J., Mayer, W. E. and Sommer, R. J. (2010). Haplotype diversity of the nematode Pristionchus pacificus on Réunion in the Indian Ocean suggests multiple independent invasions. Biological Journal of the Linnean Society 100, 170179.CrossRefGoogle Scholar
Hodgkin, J. (1983). Male phenotypes and mating efficiency in Caenorhabditis elegans . Genetics 103, 4364.Google Scholar
Hodgkin, J. (2002). Exploring the envelope. Systematic alteration in the sex-determination system of the nematode Caenorhabditis elegans . Genetics 162, 767780.CrossRefGoogle ScholarPubMed
Hodgkin, J., Horvitz, H. R. and Brenner, S. (1979). Nondisjunction mutants of the nematode Caenorhabditis elegans . Genetics 91, 6794.Google Scholar
Holterman, M., van der Wurff, A., van den Elsen, S., van Megen, H., Bongers, T., Holovachov, O., Bakker, J. and Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 17921800.Google Scholar
Holterman, M., Rybarczyk, K., van den Elsen, S., van Megen, H., Mooyman, P., Santiago, R. P., Bongers, T., Bakker, J. and Helder, J. (2008). A ribosomal DNA-based framework for the detection and quantification of stress-sensitive nematode families in terrestrial habitats. Molecular Ecology Resources 8, 2334. doi: 10.1111/j.1471–8286.2007.01963.x.Google Scholar
Kulkarni, A., Dyka, A., Nemetschke, L., Grant, W. N. and Streit, A. (2013). Parastrongyloides trichosuri suggests that XX/XO sex determination is ancestral in Strongyloididae (Nematoda). Parasitology 140, 18221830. doi: 10.1017/S0031182013001315.Google Scholar
Lee, D. L. (2002). The Biology of Nematodes. Taylor & Francis, London, UK.Google Scholar
Lucchesi, J. C., Kelly, W. G. and Panning, B. (2005). Chromatin remodeling in dosage compensation. Annual Review of Genetics 39, 615651.CrossRefGoogle ScholarPubMed
Mackerras, M. J. (1959). Strongyloides and Parastrongyloides (Nematoda: Rhabdiasoidea) in Australian marsupials. Australian Journal of Zoology 7, 87104.Google Scholar
Müller, F., Wicky, C., Spicher, A. and Tobler, H. (1991). New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin diminution in Ascaris lumbricoides . Cell 67, 815822.Google Scholar
Nemetschke, L., Eberhardt, A. G., Hertzberg, H. and Streit, A. (2010 a). Genetics, chromatin diminution, and sex chromosome evolution in the parasitic nematode genus Strongyloides . Current Biology 20, 16871696.Google Scholar
Nemetschke, L., Eberhardt, A. G., Viney, M. E. and Streit, A. (2010 b). A genetic map of the animal-parasitic nematode Strongyloides ratti . Molecular and Biochemical Parasitology 169, 124127.Google Scholar
Nigon, V. and Roman, E. (1952). Le déterminisme du sexe et le development cyclique de Strongyloides ratti . Bulletin biologique de la France et de la Belgique 86, 404448.Google Scholar
Nolan, T. J. and Schad, G. A. (1992). Cryopreservation of infective third-stage larvae of Strongyloides ratti . Journal of the Helminthological Society of Washington 59, 135140.Google Scholar
Nolan, T. J., Aikens, L. M. and Schad, G. A. (1988). Cryopreservation of first-stage and infective third-stage larvae of Strongyloides stercoralis . Journal of Parasitology 74, 387391.CrossRefGoogle ScholarPubMed
Ogawa, A., Streit, A., Antebi, A. and Sommer, R. J. (2009). A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Current Biology 19, 6771.Google Scholar
Ohta, T. (1996). The current significance and standing of neutral and neutral theories. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 18, 673677; discussion 683. doi: 10.1002/bies.950180811.Google Scholar
Osche, G. (1962). Das Praeadaptationsphänomen und seine Bedeutung für die Evolution. Zoologischer Anzeiger 169, 1449.Google Scholar
Phillips, C. M. and Dernburg, A. F. (2006). A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans . Developmental Cell 11, 817829. doi: 10.1016/j.devcel.2006.09.020.Google Scholar
Pires-daSilva, A. (2007). Evolution of the control of sexual identity in nematodes. Seminars in Cell and Developmental Biology 18, 362370.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.Google Scholar
Poulin, R. and Randhawa, H. S. (2014). Evolution of parasitism along convergent lines: from ecology to genomics. Parasitology, in press. doi: 10.1017/S0031182013001674.Google Scholar
Riddle, D. L. and Albert, P. S. (1997). Genetic and environmental regulation of dauer larva development. In C. Elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R.), pp. 739768. Cold Spring Harbor Laboratory Press, New York, NY, USA.Google Scholar
Sarre, S. D., Georges, A. and Quinn, A. (2004). The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26, 639645.Google Scholar
Schaner, C. E. and Kelly, W. G. (2006). Germline chromatin (24 January 2006). In WormBook. doi: 10.1895/wormbook.1.73.1. www.wormbook.org.Google Scholar
Schön, I., Martens, K. and Van Dijk, P. J. (2009). Lost Sex: The Evolutionary Biology of Parthenogensis. Springer, Berlin, Germany.Google Scholar
Schwander, T., Vuilleumier, S., Dubman, J. and Crespi, B. J. (2010). Positive feedback in the transition from sexual reproduction to parthenogenesis. Proceedings of the Royal Society B: Biological Sciences 277, 14351442.CrossRefGoogle ScholarPubMed
Shakes, D. C., Neva, B. J., Huynh, H., Chaudhuri, J. and Pires-daSilva, A. (2011). Asymmetric spermatocyte division as a mechanism for controlling sex ratios. Nature Communications 2, 157. doi: 10.1038/ncomms1160.Google Scholar
Shao, H., Li, X., Nolan, T. J., Massey, H. C. Jr., Pearce, E. J. and Lok, J. B. (2012). Transposon-mediated chromosomal integration of transgenes in the parasitic nematode Strongyloides ratti and establishment of stable transgenic lines. PLoS Pathogens 8, e1002871. doi: 10.1371/journal.ppat.1002871.Google Scholar
Sommer, R. J. (2009). The future of evo-devo: model systems and evolutionary theory. Nature Reviews Genetics 10, 416422.Google Scholar
Sommer, R. J. and Ogawa, A. (2011). Hormone signaling and phenotypic plasticity in nematode development and evolution. Current Biology 21, R758766. doi: 10.1016/j.cub.2011.06.034.Google Scholar
Speare, R. (1989). Identification of species of Strongyloides. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 1183. Taylor & Francis, London, UK.Google Scholar
Streit, A. (2008). Reproduction in Strongyloides (Nematoda): a life between sex and parthenogenesis. Parasitology 135, 285294.Google Scholar
Streit, A. (2012). Silencing by throwing away: a role for chromatin diminutioning. Developmental Cell 23, 918919.Google Scholar
Tobler, H. and Müller, F. (2001). Chromatin diminution. In Encyclopedia of Life Sciences, John Wiley & Sons, Chichester, UK. doi: 10.1038/npg.els.0001181. www.els.net/.Google Scholar
Triantaphyllou, A. C. and Moncol, D. J. (1977). Cytology, reproduction, and sex determination of Strongyloides ransomi and S. papillosus . Journal of Parasitology 63, 961973.Google Scholar
Valenzuela, N. (2008). Sexual development and the evolution of sex determination. Sexual Development 2, 6472.Google Scholar
Vicoso, B. and Bachtrog, D. (2013). Reversal of an ancient sex chromosome to an autosome in Drosophila . Nature 499, 332335. doi: 10.1038/nature12235.Google Scholar
Viney, M. E. (1999). Exploiting the life cycle of Strongyloides ratti . Parasitology Today 15, 231235.Google Scholar
Viney, M. E. (2006). The biology and genomics of Strongyloides. Medical Microbiology and Immunology 195, 4954.CrossRefGoogle ScholarPubMed
Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. (23 May 2007). In WormBook. doi: 10.1895/wormbook.1.141.1. www.wormbook.org.Google Scholar
Viney, M. E., Green, L. D., Brooks, J. A. and Grant, W. N. (2002). Chemical mutagenesis of the parasitic nematode Strongyloides ratti to isolate ivermectin resistant mutants. International Journal for Parasitology 32, 16771682.Google Scholar
Wang, J., Mitreva, M., Berriman, M., Thorne, A., Magrini, V., Koutsovoulos, G., Kumar, S., Blaxter, M. L. and Davis, R. E. (2012). Silencing of germline-expressed genes by DNA elimination in somatic cells. Developmental Cell 23, 10721080. doi: 10.1016/j.devcel.2012.09.020.Google Scholar
Wang, Z., Zhou, X. E., Motola, D. L., Gao, X., Suino-Powell, K., Conneely, A., Ogata, C., Sharma, K. K., Auchus, R. J., Lok, J. B., Hawdon, J. M., Kliewer, S. A., Xu, H. E. and Mangelsdorf, D. J. (2009). Identification of the nuclear receptor DAF-12 as a therapeutic target in parasitic nematodes. Proceedings of the National Academy of Sciences USA 106, 91389143.Google Scholar
Wilkins, A. S. (1995). Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17, 7177.Google Scholar
Yamada, M., Matsuda, S., Nakazawa, M. and Arizono, N. (1991). Species-specific differences in heterogonic development of serially transferred free-living generations of Strongyloides planiceps and Strongyloides stercoralis . Journal of Parasitology 77, 592594.Google Scholar