Microsatellite and single-nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite

Journal of Evolutionary Biology

Volumn 26, Issue 5, 2013, Pages 1117-1128

  Haag, K L ^a   Sheikh Jabbari, E ^a   Ben Ami, F ^b   Ebert, D ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Asexual reproduction; Mode of transmission; Population genetic structure

Indexed keywords

MICROSATELLITE DNA;

ASEXUAL REPRODUCTION; CLUSTER ANALYSIS; CRUSTACEAN; DIVERGENCE; GENETIC MARKER; GENETIC STRUCTURE; LIFE CYCLE; LIFE HISTORY TRAIT; PARASITE; PARASITE TRANSMISSION; PHYLOGENETICS; PHYLOGEOGRAPHY; POLYMORPHISM;

ANIMAL; ARTICLE; ASEXUAL REPRODUCTION; DAPHNIA; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; MICROSPORIDIA; PHYLOGEOGRAPHY; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; DAPHNIA; HOST-PATHOGEN INTERACTIONS; MICROSATELLITE REPEATS; MICROSPORIDIA; PHYLOGEOGRAPHY; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCTION, ASEXUAL;

EUROPE; ISRAEL;

DAPHNIA; MICROSPORIDIA;

EID: 84876970870     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12125     Document Type: Article

References (74)

1. Agnew, P. & Koella, J.C. 1999. Life history interactions with environmental conditions in a host-parasite relationship and the parasite's mode of transmission. Evol. Ecol. 13: 67-91.
2. Akinbo, F.O., Okaka, C.E., Omoregie, R., Dearen, T., Leon, E.T. & Xiao, L. 2012. Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. Am. J. Trop. Med. Hyg. 86: 441-445.
3. Alby, K. & Bennett, R. 2010. Sexual reproduction in the Candida clade: cryptic cycles, diverse mechanisms, and alternative functions. Cell. Mol. Life Sci. 67: 3275-3285.
4. Avise, J.C. 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Harvard.
5. Bandelt, H.J., Forster, P., Sykes, B.C. & Richards, M.B. 1995. Mitochondrial portraits of human populations using median networks. Genetics 141: 743-753.
6. Barrett, L.G., Thrall, P.H., Burdon, J.J. & Linde, C.C. 2008a. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol. Evol. 23: 678-685.
7. Barrett, L.G., Thrall, P.H., Burdon, J.J., Nicotra, A.B. & Linde, C.C. 2008b. Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Mol. Ecol. 17: 3401-3415.
8. Blouin, M.S., Yowell, C.A., Courtney, C.H. & Dame, J.B. 1995. Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141: 1007-1014.
9. Bruns, E., Carson, M. & May, G. 2012. Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages. BMC Evol. Biol. 12: 135.
10. Burdon, J.J. & Roelfs, A.P. 1985. The effect of sexual and asexual reproduction on the isozyme structure of populations of Puccinia graminis. Phytopathology 75: 1068-1073.
11. Burdon, J.J. & Thrall, P.H. 2008. Pathogen evolution across the agro-ecological interface: implications for disease management. Evol. Appl. 1: 57-65.
12. Burt, A., Carter, D.A., Koenig, G.L., White, T.J. & Taylor, J.W. 1996. Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. PNAS 93: 770-773.
13. Carriconde, F., Gilgado, F., Arthur, I., Ellis, D., Malik, R., Van de Wiele, N. et al. 2011. Clonality and α-a recombination in the Australian Cryptococcus gattii VGII population - an emerging outbreak in Australia. PLoS ONE 6: e16936.
14. Coelho, M., Gonçalves, P. & Sampaio, J. 2011. Evidence for maintenance of sex determinants but not of sexual stages in red yeasts, a group of early diverged basidiomycetes. BMC Evol. Biol. 11: 249.
15. Cox, F.E.G. 2009. Modern Parasitology: A Textbook of Parasitology. Blackwell Science, Oxford.
16. Criscione, C.D. & Blouin, M.S. 2004. Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58: 198-202.
17. Criscione, C.D., Poulin, R. & Blouin, M.S. 2005. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 14: 2247-2257.
18. Daverdin, G., Rouxel, T., Gout, L., Aubertot, J.-N., Fudal, I., Meyer, M. et al. 2012. Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog. 8: e1003020.
19. Davies, C.M., Webster, J.P. & Woolhous, M.E. 2001. Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite, Proc. Biol. Sci. 268: 251-257.
20. De Gelas, K. & De Meester, L. 2005. Phylogeography of Daphnia magna in Europe. Mol. Ecol. 14: 753-764.
21. Decaestecker, E., Declerck, S., De Meester, L. & Ebert, D. 2005. Ecological implications of parasites in natural Daphnia populations. Oecologia 144: 382-390.
22. Dunn, A.M. & Smith, J.E. 2001. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 3: 381-388.
23. Ebert, D. 1998. Experimental evolution of parasites. Science 282: 1432-1436.
24. Ebert, D., Hottinger, J.W. & Pajunen, V.I. 2001. Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82: 3417-3434.
25. Ebert, D., Altermatt, F. & Lass, S. 2007. A short term benefit for outcrossing in a Daphnia metapopulation in relation to parasitism. J. R. Soc. Interface 4: 777-785.
26. Enzel, Y., Amit, R., Dayan, U., Crouvi, O., Kahana, R., Ziv, B. et al. 2008. The climatic and physiographic controls of the eastern Mediterranean over the late Pleistocene climates in the southern Levant and its neighboring deserts. Global Planet. Change 60: 165-192.
27. Excoffier, L., Smouse, P.E. & Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
28. Excoffier, L., Laval, G. & Schneider, S. 2007. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. 2005: 47-50.
29. Feng, Y., Li, N., Dearen, T., Lobo, M.L., Matos, O., Cama, V. et al. 2011. Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi. Appl. Environ. Microbiol. 77: 4822-4828.
30. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Marine Biol. Biotechnol. 3: 294-299.
31. Goren, L. & Ben-Ami, F. 2013. Ecological correlates between cladocerans and their endoparasites from permanent and rain pools: patterns in community composition and diversity. Hydrobiologia 701: 13-23.
32. Haag, K.L., Larsson, J.I.R., Refardt, D. & Ebert, D. 2011. Cytological and molecular description of Hamiltosporidium tvaerminnensis gen. et sp. nov., a microsporidian parasite of Daphnia magna, and establishment of Hamiltosporidium magnivora comb. nov. Parasitology 138: 447-462.
33. Haag, K.L., Traunecker, E. & Ebert, D. 2013. Single nucleotide polymorphisms of two closely related microsporidian parasites suggest a clonal population expansion after the last glaciation. Mol. Ecol. 22: 314-326.
34. Harff, J., Endler, R., Emelyanov, E., Kotov, S., Leipe, T., Moros, M. et al. 2011. Late Quaternary climate variations reflected in Baltic Sea sediments. In: The Baltic Sea Basin (J. Harff, S. Björck, P. Hoth, eds), pp. 99-132. Springer, Berlin.
35. Heitman, J. 2010. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8: 86-99.
36. Hewitt, G.M. 2001. Speciation, hybrid zones and phylogeography - or seeing genes in space and time. Mol. Ecol. 10: 537-549.
37. Ironside, J.E. 2007. Multiple losses of sex within a single genus of Microsporidia. BMC Evol. Biol. 7: 48.
38. Judson, O.P. & Normark, B.B. 1996. Ancient asexual scandals. Trends Ecol. Evol. 11: 41-46.
39. Kearney, M. 2005. Hybridization, glaciation and geographical parthenogenesis. Trends Ecol. Evol. 20: 495-502.
40. Koella, J.C. & Agnew, P. 1999. A correlated response of a parasite's virulence and life cycle to selection on its host's life history. J. Evol. Biol. 12: 70-79.
41. Kofler, R., Schlötterer, C. & Lelley, T. 2007. SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics 23: 1683-1685.
42. Lass, S. & Ebert, D. 2006. Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proc. Biol. Sci. 273: 199-206.
43. Lass, S., Hottinger, J., Fabbro, T. & Ebert, D. 2011. Converging seasonal prevalence dynamics in experimental epidemics. BMC Ecol. 11: 14.
44. Li, W., Cama, V., Feng, Y., Gilman, R.H., Bern, C., Zhang, X. et al. 2012. Population genetic analysis of Enterocytozoon bieneusi in humans. Int. J. Parasitol. 42: 287-293.
45. Librado, P. & Rozas, J. 2009. DnaSP V5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
46. MacLeod, A., Tait, A. & Turner, C.M. 2001. The population genetics of Trypanosoma brucei and the origin of human infectivity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 1035-1044.
47. Mangin, K.L., Lipsitch, M. & Ebert, D. 1995. Virulence and transmission modes of two microsporidia in Daphnia magna. Parasitology 111: 133-142.
48. Mathis, A., Weber, R. & Deplazes, P. 2005. Zoonotic potential of the Microsporidia. Clin. Microbiol. Rev. 18: 423-445.
49. Maynard-Smith, J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge.
50. Maynard-Smith, J., Smith, N.H., O'Rourke, M. & Spratt, B.G. 1993. How clonal are Bacteria? Proc. Natl Acad. Sci. USA 90: 4384-4388.
51. McCoy, K.D., Boulinier, T., Tirard, C. & Michalakis, Y. 2003. Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57: 288-296.
52. Nemri, A., Barrett, L.G., Laine, A.-L., Burdon, J.J. & Thrall, P.H. 2012. Population processes at multiple spatial scales maintain diversity and adaptation in the Linum marginale - Melampsora lini association. PLoS ONE 7: e41366.
53. O'Mahony, E.M., Tay, W.T. & Paxton, R.J. 2007. Multiple rRNA variants in a single spore of the microsporidian Nosema bombi. J. Eukaryot. Microbiol. 54: 103-109.
54. Pajunen, V.I. & Pajunen, I. 2003. Long-term dynamics in rock pool Daphnia metapopulations. Ecography 26: 731-738.
55. Paland, S., Colbourne, J.K. & Lynch, M. 2005. Evolutionary history of contagious asexuality in Daphnia pulex. Evolution 59: 800-813.
56. Poulin, R. & Cribb, T.H. 2002. Trematode life cycles: short is sweet? Trends Parasitol. 18: 176-183.
57. Pritchard, J.K., Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
58. Rauch, G., Kalbe, M. & Reusch, T.B.H. 2005. How a complex life cycle can improve a parasite's sex life. J. Evol. Biol. 18: 1069-1075.
59. Reetz, J., Nöckler, K., Reckinger, S., Vargas, M.M., Weiske, W. & Broglia, A. 2009. Identification of Encephalitozoon cuniculi genotype III and two novel genotypes of Enterocytozoon bieneusi in swine. Parasitol. Int. 58: 285-292.
60. Sandrock, C. & Vorburger, C. 2011. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Curr. Biol. 21: 433-437.
61. Sibley, L.D. & Ajioka, J.W. 2008. Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu. Rev. Microbiol. 62: 329-351.
62. Smith, J.E. 2009. The ecology and evolution of microsporidian parasites. Parasitology 136: 1901-1914.
63. Sun, S. & Heitman, J. 2011. Is sex necessary? BMC Biol. 9: 56.
64. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
65. Tibayrenc, M. & Ayala, F.J. 2002. The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol. 18: 405-410.
66. Tibayrenc, M. & Ayala, F.J. 2012. Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proc. Natl. Acad. Sci. USA 109: E3305-E3313.
67. Vercken, E., Fontaine, M.C., Gladieux, P., Hood, M.E., Jonot, O. & Giraud, T. 2010. Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathog. 6: e1001229.
68. Vizoso, D.B. & Ebert, D. 2004. Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128: 31-38.
69. Vizoso, D.B., Lass, S. & Ebert, D. 2005. Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 130: 501-509.
70. Wendte, J.M., Miller, M.A., Lambourn, D.M., Magargal, S.L., Jessup, D.A. & Grigg, M.E. 2010. Self-Mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii. PLoS Genet. 6: e1001261.
71. Wolinska, J., Giessler, S. & Koerner, H. 2009. Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Appl. Environ. Microbiol. 75: 7051-7059.
72. Wolinska, J., Spaak, P., Koerner, H., Petrusek, A., Seda, J. & Giessler, S. 2011. Transmission mode affects the population genetic structure of Daphnia parasites. J. Evol. Biol. 24: 265-273.
73. Xhaard, C., Fabre, B., Andrieux, A., Gladieux, P., Barrès, B., Frey, P. et al. 2011. The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication. Mol. Ecol. 20: 2739-2755.
74. Xiao, L., Li, L., Visvesvara, G.S., Moura, H., Didier, E.S. & Lal, A.A. 2001. Genotyping Encephalitozoon cuniculi by multilocus analyses of genes with repetitive sequences. J. Clin. Microbiol. 39: 2248-2253.