BACKGROUND: The population structure of cyclical parthenogens such as water fleas is strongly influenced by the frequency of alternations between sexual and asexual (parthenogenetic) reproduction, which may differ among populations and species. We studied genetic variation within six populations of two closely related species of water fleas of the genus Daphnia (Crustacea, Cladocera). D. galeata and D. longispina both occur in lakes in the Tatra Mountains (Central Europe), but their populations show distinct life history strategies in that region. In three studied lakes inhabited by D. galeata, daphnids overwinter under the ice as adult females. In contrast, in lakes inhabited by D. longispina, populations apparently disappear from the water column and overwinter as dormant eggs in lake sediments. We investigated to what extent these different strategies lead to differences in the clonal composition of late summer populations. RESULTS: Analysis of genetic variation at nine microsatellite loci revealed that clonal richness (expressed as the proportion of different multilocus genotypes, MLGs, in the whole analysed sample) consistently differed between the two studied species. In the three D. longispina populations, very high clonal richness was found (MLG/N ranging from 0.97 to 1.00), whereas in D. galeata it was much lower (0.05 to 0.50). The dominant MLGs in all D. galeata populations were heterozygous at five or more loci, suggesting that such individuals all represented the same clonal lineages rather than insufficiently resolved groups of different clones. CONCLUSIONS: The low clonal diversities and significant deviations from Hardy-Weinberg equilibrium in D. galeata populations were likely a consequence of strong clonal erosion over extended periods of time (several years or even decades) and the limited influence of sexual reproduction. Our data reveal that populations of closely related Daphnia species living in relatively similar habitats (permanent, oligotrophic mountain lakes) within the same region may show strikingly different genetic structures, which most likely depend on their reproductive strategy during unfavourable periods. We assume that similar impacts of life history on population structures are also relevant for other cyclical parthenogen groups. In extreme cases, prolonged clonal erosion may result in the dominance of a single clone within a population, which might limit its microevolutionary potential if selection pressures suddenly change.

Department of Ecology Faculty of Science Charles University Prague Prague Czech Republic

Zobrazit více v PubMed

De Meester L, Gómez A, Simon JC. In: Evolution from Molecules to Ecosystems. Moya A, Font E, editor. Oxford University Press; 2004. Evolutionary and ecological genetics of cyclical parthenogens; pp. 122–134.

Decaestecker E, De Meester L, Mergeay J. In: Lost Sex: The Evolutionary Biology of Parthenogenesis. Schön I, Martens K, van Dijk P, editor. Springer; 2009. Cyclical parthenogenesis in Daphnia: sexual versus asexual reproduction; pp. 295–316.

Gyllström M, Hansson LA. Dormancy in freshwater zooplankton: Induction, termination and the importance of benthic-pelagic coupling. Aquat Sci. 2004;66:274–295.

De Meester L. Local genetic differentiation and adaptation in freshwater zooplankton populations: patterns and processes. Ecoscience. 1996;3:385–399.

De Meester L, Vanoverbeke J, De Gelas K, Ortells R, Spaak P. Genetic structure of cyclic parthenogenetic zooplankton populations - a conceptual framework. Arch Hydrobiol. 2006;167:217–244. doi: 10.1127/0003-9136/2006/0167-0217. DOI

Vanoverbeke J, De Meester L. Clonal erosion and genetic drift in cyclical parthenogens - the interplay between neutral and selective processes. J Evol Biol. 2010;23:997–1012. doi: 10.1111/j.1420-9101.2010.01970.x. PubMed DOI

De Meester L, Vanoverbeke J. An uncoupling of male and sexual egg production leads to reduced inbreeding in the cyclical parthenogen Daphnia. Proc R Soc Lond B. 1999;266:2471–2477. doi: 10.1098/rspb.1999.0948. PubMed DOI PMC

Vanoverbeke J, De Meester L. Among-populational genetic differentiation in the cyclical parthenogen Daphnia magna (Crustacea, Anomopoda) and its relation to geographic distance and clonal diversity. Hydrobiologia. 1997;360:135–142. doi: 10.1023/A:1003160903708. DOI

Brendonck L, De Meester L. Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia. 2003;491:65–84.

Cáceres CE, Hartway C, Paczlot KA. Inbreeding depression varies with investment in sex in a facultative parthenogen. Evolution. 2009;63:2474–2480. doi: 10.1111/j.1558-5646.2009.00707.x. PubMed DOI

Gómez A, Carvalho GR. Sex, parthenogenesis and the genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank population. Mol Ecol. 2000;9:203–214. doi: 10.1046/j.1365-294x.2000.00849.x. PubMed DOI

Sunnucks P, DeBarro PJ, Lushai G, Maclean N, Hales D. Genetic structure of an aphid studied using microsattelites: Cyclic parthenogenesis, differentiated lineages and host speciation. Mol Ecol. 1997;6:1059–1073. doi: 10.1046/j.1365-294X.1997.00280.x. PubMed DOI

Hartnett DC, Bazzaz FA. The genet and ramet population dynamics of Solidago canadensis in an abandoned field. J Ecol. 1985;73:407–413. doi: 10.2307/2260483. DOI

Janko K, Drozd P, Flegr J, Pannell JR. Clonal turnover versus clonal decay: a null model for observed patterns of asexual longevity, diversity and distribution. Evolution. 2008;62:1264–1270. doi: 10.1111/j.1558-5646.2008.00359.x. PubMed DOI

Janko K, Drozd P, Eisner J. Do clones degenerate over time? Explaining the genetic variability of asexuals through population genetic models. Biology Direct. 2011;6:17. doi: 10.1186/1745-6150-6-17. PubMed DOI PMC

Lampert W, Lampert KP, Larsson P. Coexisting overwintering strategies in Daphnia pulex: A test of genetic differences and growth responses. Limnol Oceanogr. 2010;55:1893–1900. doi: 10.4319/lo.2010.55.5.1893. DOI

Zaffagnini F. In: Daphnia. Peters RH, de Bernardi R, editor. Vol. 45. 1987. Reproduction in Daphnia; pp. 245–284. Mem Ist Ital Idrobiol.

Jankowski T, Straile D. Allochronic differentiation among Daphnia species, hybrids and backcrosses: the importance of sexual reproduction for population dynamics and genetic architecture. J Evol Biol. 2004;17:312–321. PubMed

Zeis B, Horn W, Gigengack U, Koch M, Paul RJ. A major shift in Daphnia genetic structure after the first ice-free winter in a German reservoir. Freshw Biol. 2010;55:2296–2304.

Spaak P. Temporal changes in the genetic structure of the Daphnia species complex in Tjeukemeer, with evidence for backcrossing. Heredity. 1996;76:539–548. doi: 10.1038/hdy.1996.77. DOI

Thielsch A, Brede N, Petrusek A, De Meester L, Schwenk K. Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia. Mol Ecol. 2009;18:1616–1628. doi: 10.1111/j.1365-294X.2009.04130.x. PubMed DOI

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;19:4168–4178. doi: 10.1111/j.1365-294X.2010.04807.x. PubMed DOI

Petrusek A, Hobæk A, Nilssen JP, Skage M, Černý M, Brede N, Schwenk K. A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda) Zool Scr. 2008;37:507–519. doi: 10.1111/j.1463-6409.2008.00336.x. DOI

Petrusek A, Černý M, Mergeay J, Schwenk K. Daphnia in the Tatra Mountain lakes: multiple colonisation and hidden species diversity revealed by molecular markers. Fundam Appl Limnol. 2007;169:279–291. doi: 10.1127/1863-9135/2007/0169-0279. DOI

de Senertpont Domis LN, Mooij WM, Hülsmann S, van Nes EH, Scheffer M. Can overwintering versus diapausing strategy in Daphnia determine match-mismatch events in zooplankton-algae interactions? Oecologia. 2007;150:682–698. PubMed

Rellstab C, Spaak P. Lake origin determines Daphnia population growth under winter conditions. J Plankton Res. 2009;31:261–271.

Hamrová E. Ph.D. thesis. Department of Ecology, Faculty of Science, Charles University in Prague; 2011. Genetic structure of the Daphnia longispina complex in European mountain lakes.

Cáceres CE, Tessier AJ. To sink or swim: Variable diapause strategies among Daphnia species. Limnol Oceanogr. 2004;49:1333–1340. doi: 10.4319/lo.2004.49.4_part_2.1333. DOI

Gliwicz ZM, Slusarczyk A, Slusarczyk M. Life history synchronization in a long-lifespan single-cohort Daphnia population in a fishless alpine lake. Oecologia. 2001;128:368–378. doi: 10.1007/s004420100673. PubMed DOI

Aguilera X, Mergeay J, Wollebrants A, Declerck S, De Meester L. Asexuality and polyploidy in Daphnia from the tropical Andes. Limnol Oceanogr. 2007;52:2079–2088. doi: 10.4319/lo.2007.52.5.2079. DOI

Dufresne F, Marková S, Vergilino V, Ventura M, Kotlík P. Diversity in the reproductive modes of European Daphnia pulicaria deviates from the geographical parthenogenesis. PLoS ONE. 2011;6:e20049. doi: 10.1371/journal.pone.0020049. PubMed DOI PMC

Hamrová E, Goliáš V, Petrusek A. Identifying century-old long-spined Daphnia: species replacement in a mountain lake characterised by paleogenetic methods. Hydrobiologia. 2010;643:97–106. doi: 10.1007/s10750-010-0127-9. DOI

Lityński A. Revision der Cladocerenfauna der Tatra-Seen. I. Teil. Daphnidae. Bull int Acad Sci Cracovie, Cl Sci Math Nat, ser B. 1913;1913:566–623.

Brede N, Sandrock C, Straile D, Spaak P, Jankowski T, Streit B, Schwenk K. The impact of human-made ecological changes on the genetic architecture of Daphnia species. Proc Natl Acad Sci USA. 2009;106:4758–4763. doi: 10.1073/pnas.0807187106. PubMed DOI PMC

Boileau MG, Hebert PDN, Schwartz SS. Non-equilibrium gene frequency divergence: persistent founder effect in natural populations. J Evol Biol. 1992;5:25–39. doi: 10.1046/j.1420-9101.1992.5010025.x. DOI

Wolinska J, Spaak P. The cost of being common: evidence from natural Daphnia populations. Evolution. 2009;63:1893–1901. doi: 10.1111/j.1558-5646.2009.00663.x. PubMed DOI

De Meester L, Gómez A, Okamura B, Schwenk K. The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol. 2002;23:121–135. doi: 10.1016/S1146-609X(02)01145-1. DOI

Mergeay J, Vanoverbeke J, Verschuren D, De Meester L. Extinction, recolonisation and dispersal through time in a planktonic crustacean. Ecology. 2007;88:3032–3043. doi: 10.1890/06-1538.1. PubMed DOI

Hořická Z, Stuchlík E, Hudec I, Černý M, Fott J. Acidification and the structure of crustacean zooplankton in mountain lakes: The Tatra Mountains (Slovakia, Poland) Biologia. 2006;61:S121–S134. doi: 10.2478/s11756-006-0125-6. DOI

Blažka P. Některé fysiologické charakteristiky tatranských korýšů [Some physiological characteristics of the Tatra crustaceans] Zbor prác o Tatr Nár parku. 1964;7:227–231.

Schwenk K, Sand A, Boersma M, Brehm M, Mader E, Offerhaus D, Spaak P. Genetic markers, genealogies and biogeographic patterns in the Cladocera. Aquat Ecol. 1998;32:37–51. doi: 10.1023/A:1009939901198. DOI

Brede N, Thielsch A, Sandrock C, Spaak P, Keller B, Streit B, Schwenk K. Microsatellite markers for European Daphnia. Mol Ecol Notes. 2006;6:536–539. doi: 10.1111/j.1471-8286.2005.01218.x. DOI

Belkhir 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; 1996. http://www.genetix.univ-montp2.fr

Chao A, Shen T-J. Program SPADE (Species Prediction And Diversity Estimation) 2003. http://chao.stat.nthu.edu.tw

Nielsen EE, Bach LA, Kotlicki P. HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes. 2006;6:971–973. doi: 10.1111/j.1471-8286.2006.01433.x. DOI

Meirmans PG, Van Tienderen PH. GenoType and GenoDive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes. 2004;4:792–794. doi: 10.1111/j.1471-8286.2004.00770.x. DOI

Rogstad SH, Keane B, Beresh J. Genetic variation across VNTR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecol. 2002;161:111–121. doi: 10.1023/A:1020301011283. DOI

Jost L. GST and its relatives do not measure differentiation. Mol Ecol. 2008;17:4015–4026. doi: 10.1111/j.1365-294X.2008.03887.x. PubMed DOI

Crawford NG. SMOGD: Software for the measurement of genetic diversity. Mol Ecol Res. 2010;10:556–557. doi: 10.1111/j.1755-0998.2009.02801.x. PubMed DOI

Ertl M. Príspevok k poznaniu zimného zooplanktonu Štrbského plesa [Contribution to the knowledge of winter zooplankton of Štrbské pleso lake] Biologia. 1963;18:787–791.

Kneslová P, Dargocká J, Stuchlík E. Zooplankton osmi různě acidifikovaných ples ve Vysokých Tatrách [Zooplankton of eight High Tatra Mountain lakes in different stage of acidification] Štúd o Tatr nár parku. 1997;2:123–134.

Kopáček J, Stuchlík E, Hardekopf D. Chemical composition of the Tatra Mountain lakes: Recovery from acidification. Biologia. 2006;61:S21–S33. doi: 10.2478/s11756-006-0117-6. DOI

Cytonuclear diversity and shared mitochondrial haplotypes among Daphnia galeata populations separated by seven thousand kilometres

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