Population structure of a microparasite infecting Daphnia: Spatio-temporal dynamics

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Wolinska, Justyna ^a   Petrusek, Adam ^b   Yin, Mingbo ^c   Koerner, Henrike ^d   Seda, Jaromir ^e   Giessler, Sabine ^f  

^a LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^b CHARLES UNIVERSITY   (Czech Republic)

^c FUDAN UNIVERSITY   (China)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e INSTITUTE OF HYDROBIOLOGY   (Czech Republic)

^f UNIVERSITY OF MUNICH   (Germany)

Author keywords

Caullerya mesnili; Host Parasite coevolution; ITS region

Indexed keywords

COEVOLUTION; CRUSTACEAN; DATA SET; DISPERSAL; EPIDEMIOLOGY; GENETIC MARKER; GENETIC VARIATION; GENOTYPE; HOST-PARASITE INTERACTION; PARASITIC DISEASE; POLYMORPHISM; POPULATION GENETICS; POPULATION STRUCTURE; SPATIOTEMPORAL ANALYSIS; TEMPORAL VARIATION;

DAPHNIA; DAPHNIA LONGISPINA; ICHTHYOSPOREA;

FRESH WATER; RIBOSOMAL SPACER DNA;

ANIMAL; CLASSIFICATION; CZECH REPUBLIC; DAPHNIA; EUKARYOTE; EVOLUTION; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; PARASITOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; CZECH REPUBLIC; DAPHNIA; DNA, RIBOSOMAL SPACER; EUKARYOTA; FRESH WATER; GENETIC VARIATION; MOLECULAR SEQUENCE DATA;

EID: 84923932444     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-014-0247-3     Document Type: Article

References (76)

1. Koskella B, Lively CM: Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution 2007, 61(1):152-159.
2. Schulte RD, Makus C, Hasert B, Michiels NK, Schulenburg H: Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proc R Soc B 2011, 278(1719):2832-2839.
3. Morran LT, Schmidt OG, Gelarden IA, Parrish RC II, Lively CM: Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 2011, 333(6039):216-218.
4. Wolinska J, King KC: Environment can alter selection in host-parasite interactions. Trends Parasitol 2009, 25(5):236-244.
5. Mostowy R, Engelstadter J: The impact of environmental change on host-parasite coevolutionary dynamics. Proc R Soc B 2011, 278(1716):2283-2292.
6. Little TJ, Ebert D: Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera). J Anim Ecol 1999, 68(1):134-149.
7. Wolinska J, Spaak P: The cost of being common: evidence from natural Daphnia populations. Evolution 2009, 63(7):1893-1901.
8. Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L: Host-parasite "Red Queen" dynamics archived in pond sediment. Nature 2007, 400:870-873.
9. Gsell AS, de Senerpont Domis LN, Verhoeven KJF, Van Donk E, Ibelings BW: Chytrid epidemics may increase genetic diversity of a diatom springbloom. ISME J 2013, 7(10):2057-2059.
10. Vernon JG, Okamura B, Jones CS, Noble LR: Temporal patterns of clonality and parasitism in a population of freshwater bryozoans. Proc R Soc B 1996, 263(1375):1313-1318.
11. Siemens DH, Roy BA: Tests for parasite-mediated frequency-dependent selection in natural populations of an asexual plant species. Evol Ecol 2005, 19(4):321-338.
12. Burdon JJ, Thompson JN: Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. J Ecol 1995, 83(2):199-206.
13. Jokela J, Dybdahl ME, Lively CM: The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am Nat 2009, 174(S1):S43-S53.
14. King KC, Delph LF, Jokela J, Lively CM: The geographic mosaic of sex and the Red Queen. Curr Biol 2009, 19(17):1438-1441.
15. Jaenike J: A hypothesis to account for the maintenance of sex within populations. Evol Theory 1978, 3:191-194.
16. Hamilton WD: Sex versus non-sex versus parasite. Oikos 1980, 35(2):282-290.
17. Sarkar SF, Guttman DS: Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 2004, 70(4):1999-2012.
18. Orjuela-Sanchez P, Da Silva-Nunes M, Da Silva NS, Scopel KKG, Goncalves RM, Malafronte RS, Ferreira MU: Population dynamics of genetically diverse Plasmodium falciparum lineages: community-based prospective study in rural Amazonia. Parasitology 2009, 136(10):1097-1105.
19. Ghedin E, Sengamalay NA, Shumway M, Zaborsky J, Feldblyum T, Subbu V, Spiro DJ, Sitz J, Koo H, Bolotov P, Dernovoy D, Tatusova T, Bao Y, St George K, Taylor J, Lipman DJ, Fraser CM, Taubenberger JK, Salzberg SL: Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 2005, 437(7062):1162-1166.
20. Schall JJ, Denis KMS: Microsatellite loci over a thirty-three year period for a malaria parasite (Plasmodium mexicanum): bottleneck in effective population size and effect on allele frequencies. Parasitology 2013, 140(1):21-28.
21. Thrall PH, Laine A-L, Ravensdale M, Nemri A, Dodds PN, Barrett LG, Burdon JJ: Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol Lett 2012, 15(5):425-435.
22. Flor HH: The complementary genetic systems in flax and flax rust. Adv Genet 1956, 8:29-54.
23. Dodds PN, Rathjen JP: Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 2010, 11(8):539-548.
24. Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I: Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc B 1996, 263(1373):1003-1009.
25. Gandon S: Local adaptation and the geometry of host-parasite coevolution. Ecol Lett 2002, 5(2):246-256.
26. Lively CM: Host-parasite coevolution and sex: do interactions between biological enemies maintain genetic variation and cross-fertilization? Bioscience 1996, 46:107-114.
27. Duffy MA, Ochs JH, Penczykowski RM, Civitello DJ, Klausmeier CA, Hall SR: Ecological context influences epidemic size and parasite-driven evolution. Science 2012, 335(6076):1636-1638.
28. Duncan A, Little TJ: Parasite-driven genetic change in a natural population of Daphnia. Evolution 2007, 64(4):796-803.
29. Yin M, Petrusek A, Seda J, Wolinska J: Fine-scale genetic analysis of Daphnia host populations infected by two virulent parasites - strong fluctuations in clonal structure at small temporal and spatial scales. Int J Parasitol 2012, 42(1):115-121.
30. Schwarzenberger A, D'Hondt S, Vyverman W, von Elert E: Seasonal succession of cyanobacterial protease inhibitors and Daphnia magna genotypes in a eutrophic Swedish lake. Aquat Sci 2013, 75(3):433-445.
31. Haag KL, Ebert D: Single-nucleotide polymorphisms of two closely related microsporidian parasites suggest a clonal population expansion after the last glaciation. Mol Ecol 2012, 22(2):314-326.
32. Haag KL, Sheikh-Jabbari E, Ben-Ami F, Ebert D: Microsatellite and singlenucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite. J Evol Biol 2013, 26(5):1117-1128.
33. Schwenk K, Spaak P: Evolutionary and ecological consequences of interspecific hybridization in cladocerans. Experientia 1995, 51:465-481.
34. Petrusek A, Hobaek A, Nilssen JP, Skage M, Cerny M, Brede N, Schwenk K: A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda). Zool Scr 2008, 37(5):507-519.
35. Wolinska J, Seda J, Koerner H, Smilauer P, Petrusek A: Spatial variation of Daphnia parasite load within individual water bodies. J Plankton Res 2011, 33(8):1284-1294.
36. Lohr J, Laforsch C, Koerner H, Wolinska J: A Daphnia parasite (Caullerya mesnili) constitutes a new member of the Ichthyosporea, a group of protists near the animal-fungi divergence. J Eukaryot Microbiol 2010, 53(4):328-336.
37. Wolinska J, Bittner K, Ebert D, Spaak P: The coexistence of hybrid and parental Daphnia : the role of parasites. Proc R Soc B 2006, 273:1977-1983.
38. Wolinska J, Spaak P, Petrusek A, Koerner H, Seda J, Giessler S: Transmission mode affects the population genetic structure of Daphnia parasites. J Evol Biol 2011, 24(2):265-273.
39. Bittner K, Rothhaupt KO, Ebert D: Ecological interactions of the microparasite Caullerya mesnili and its host Daphnia galeata. Limnol Oceanogr 2002, 47(1):300-305.
40. Giessler S, Wolinska J: Capturing the population structure of microparasites: using ITS-sequence data and a pooled DNA approach. Mol Ecol Res 2013, 13(5):918-928.
41. Ventura M, Petrusek A, Miro A, Hamrová E, Bunay D, De Meester L, Mergeay J: Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential. Mol Ecol 2014, 23(5):1014-1027.
42. Hamrová E, Mergeay J, Petrusek A: Strong differences in the clonal variation of two Daphnia species from mountain lakes affected by overwintering strategy. BMC Evol Biol 2011, 11:231.
43. Yin M, Wolinska J, Giessler S: Clonal diversity, clonal persistence and rapid taxon replacement in natural populations of species and hybrids of the Daphnia longispina complex. Mol Ecol 2010, 19(19):4168-4178.
44. Havel JE, Shurin JB: Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnol Oceanogr 2004, 49(4):1229-1238.
45. Figuerola J, Green AJ, Michot TC: Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. Am Nat 2005, 165(2):274-280.
46. Louette G, Vanoverbeke J, Ortells R, De Meester L: The founding mothers: the genetic structure of newly established Daphnia populations. Oikos 2007, 116(5):728-741.
47. Ortells R, Vanoverbeke J, Louette G, De Meester L: Colonization of Daphnia magna in a newly created pond: founder effects and secondary immigrants. Hydrobiologia 2014, 723(1):167-179.
48. Ebert D, Zschokke Rohringer CD, Carius HJ: Dose effects and densitydependent regulation of two microparasites of Daphnia magna. Oecologia 2000, 122(2):200-209.
49. Mendoza L, Taylor JW, Ajello L: The class mesomycetozoea: a group of microorganisms at the animal-fungal boundary. Annu Rev Microbiol 2002, 56:315-344.
50. Marshall WL, Berbee ML: Population-level analyses indirectly reveal cryptic sex and life history traits of Pseudoperkinsus tapetis (Ichthyosporea, Opisthokonta): a unicellular relative of the animals. Mol Biol Evol 2010, 27(9):2014-2026.
51. Schoebel CN, Tellenbach C, Spaak P, Wolinska J: Temperature effects on parasite prevalence in a natural hybrid complex. Biol Lett 2011, 7(1):108-111.
52. Agrawal A, Lively CM: Infection genetics: gene-for-gene versus matchingalleles models and all points in between. Evol Ecol Res 2002, 4(1):79-90.
53. Lythgoe KA: Effects of acquired immunity and mating strategy on the genetic structure of parasite populations. Am Nat 2002, 159(5):519-529.
54. Schmid-Hempel P, Funk CR: The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris. Parasitology 2004, 129:147-158.
55. Erler S, Popp M, Wolf S, Lattorff HMG: Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.). Ecol Evol 2012, 2(5):930-940.
56. Salathe RM, Schmid-Hempel P: The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. Plos One 2011, 6:8.
57. Seda J, Petrusek A, Machacek J, Smilauer P: Spatial distribution of the Daphnia longispina species complex and other planktonic crustaceans in the heterogeneous environment of canyon-shaped reservoirs. J Plankton Res 2007, 29(7):619-628.
58. Petrusek A, Seda J, Machacek J, Ruthova S, Smilauer P: Daphnia hybridization along ecological gradients in pelagic environments: the potential for the presence of hybrid zones in plankton. Philos Trans R Soc Lond B 2008, 363(1505):2931-2941.
59. Floate KD, Whitham TG: The hybrid bridge hypothesis: host shifting via plant hybrid swarms. Am Nat 1993, 141:651-662.
60. Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM: Parasite establishment in host communities. Ecol Lett 2003, 6(9):837-842.
61. Dobson A: Population dynamics of pathogens with multiple host species. Am Nat 2004, 164(5):S64-S78.
62. Archie EA, Ezenwa VO: Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. Int J Parasitol 2011, 41(1):89-98.
63. Andras JP, Ebert D: A novel approach to parasite population genetics: experimental infection reveals geographic differentiation, recombination and host-mediated population structure in pasteuria ramosa, a bacterial parasite of daphnia. Mol Ecol 2013, 22(4):972-986.
64. Carriconde F, Gardes M, Jargeat P, Heilmann-Clausen J, Mouhamadou B, Gryta H: Population evidence of cryptic species and geographical structure in the cosmopolitan ectomycorrhizal fungus, Tricholoma Scalpturatum. Microb Ecol 2008, 56(3):513-524.
65. Stukenbrock EH, McDonald BA: Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol Plant-Microbe Interact 2009, 22(4):371-380.
66. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J: Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 1999, 400(6745):667-671.
67. Tollenaere C, Susi H, Nokso-Koivisto J, Koskinen P, Tack A, Auvinen P, Paulin L, Frilander MJ, Lehtonen R, Laine A-L: SNP design from 454 sequencing of Podosphaera plantaginis transcriptome reveals a genetically diverse pathogen metapopulation with high levels of mixed-genotype infection. Plos One 2012, 7:12.
68. Qi W, Kaeser M, Roeltgen K, Yeboah-Manu D, Pluschke G: Genomic diversity and evolution of Mycobacterium ulcerans revealed by next-generation sequencing. PLoS Pathog 2009, 5:9.
69. Schoebel CN, Jung E, Prospero S: Development of new polymorphic microsatellite markers for three closely related plant-pathogenic Phytophthora species using 454-pyrosequencing and their potential applications. Phytopathology 2013, 103(10):1020-1027.
70. Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:91-98.
71. Clement M, Posada D, Crandall KA: TCS: a computer program to estimate gene genealogies. Mol Ecol 2000, 9(10):1657-1659.
72. Brede N, Thielsch A, Sandrock C, Spaak P, Keller B, Streit B, Schwenk K: Microsatellite markers for European Daphnia. Mol Ecol Notes 2006, 6(2):536-539.
73. Bélkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F: GENETIX 4.05, logiciel sous windows TM pour la génétique des populations. Laboratoire génome, populations, interactions, CNRS UMR 5000, université de Montpellier II, Montpellier (France). Available from URL: http://kimura.univ-montp2.fr/genetix/.
74. Anderson EC, Thompson EA: A model-based method for identifying species hybrids using multilocus genetic data. Genetics 2002, 160(3):1217-1229.
75. Excoffier L, Lischer HEL: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Res 2010, 10:564-567.
76. Rice WR: Analyzing tables of statistical tests. Evolution 1989, 43:223-225.