BACKGROUND: Genetically divergent cryptic species are frequently detected by molecular methods. These discoveries are often a byproduct of molecular barcoding studies in which fragments of a selected marker are used for species identification. Highly divergent mitochondrial lineages and putative cryptic species are even detected in intensively studied animal taxa, such as the crustacean genus Daphnia. Recently, eleven such lineages, exhibiting genetic distances comparable to levels observed among well-defined species, were recorded in the D. longispina species complex, a group that contains several key taxa of freshwater ecosystems. We tested if three of those lineages represent indeed distinct species, by analyzing patterns of variation of ten nuclear microsatellite markers in six populations. RESULTS: We observed a discordant pattern between mitochondrial and nuclear DNA, as all individuals carrying one of the divergent mitochondrial lineages grouped at the nuclear level with widespread, well-recognized species coexisting at the same localities (Daphnia galeata, D. longispina, and D. cucullata). CONCLUSIONS: A likely explanation for this pattern is the introgression of the mitochondrial genome of undescribed taxa into the common species, either in the distant past or after long-distance dispersal. The occurrence of highly divergent but rare mtDNA lineages in the gene pool of widespread species would suggest that hybridization and introgression in the D. longispina species complex is frequent even across large phylogenetic distances, and that discoveries of such distinct clades must be interpreted with caution. However, maintenance of ancient polymorphisms through selection is another plausible alternative that may cause the observed discordance and cannot be entirely excluded.

Faculty of Science Department of Biology Ferdowsi University of Mashhad Mashhad Iran

Faculty of Science Department of Ecology Charles University Prague Czechia

Institute for Environmental Sciences Molecular Ecology University of Koblenz Landau Landau in der Pfalz Germany

Zobrazit více v PubMed

Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP. A plea for DNA taxonomy. Trends Ecol Evol. 2003;18(2):70–4.

Hebert PDN, Cywinska A, Ball SL, DeWaard JR. Biological identifications through DNA barcodes. Proc R Soc Lond Ser B Biol Sci. 2003;270(1512):313–321. doi: 10.1098/rspb.2002.2218. PubMed DOI PMC

Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. P Natl Acad Sci USA. 2004;101(41):14812–14817. doi: 10.1073/pnas.0406166101. PubMed DOI PMC

Hebert PDN, Ratnasingham S, deWaard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond Ser B Biol Sci. 2003;270:S96–9. PubMed PMC

Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I. Cryptic species as a window on diversity and conservation. Trends Ecol Evol. 2007;22(3):148–155. doi: 10.1016/j.tree.2006.11.004. PubMed DOI

Pfenninger M, Schwenk K. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol Biol. 2007;7:121. PubMed PMC

Adamowicz SJ, Petrusek A, Colbourne JK, Hebert PDN, Witt JDS. The scale of divergence: a phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus. Mol Phylogenet Evol. 2009;50(3):423–36. PubMed

Petrusek A, Thielsch A, Schwenk K. Mitochondrial sequence variation suggests extensive cryptic diversity within Western Palaearctic Daphnia longispina complex. Limnol Oceanogr. 2012;57(4):1838–45.

Ishida S, Takahashi A, Matsushima N, Yokoyama J, Makino W, Urabe J, Kawata M. The long-term consequences of hybridization between the two Daphnia species, D. galeata and D. dentifera, in mature habitats. BMC Evol Biol. 2011;11:209. PubMed PMC

Zuykova EI, Bochkarev NA, Katokhin AV. Molecular genetic identification and phylogeny of Daphnia species (Crustacea, Cladocera) from water bodies of the Lake Chany basin. Russ J Genet. 2013;49(2):206–213. doi: 10.1134/S1022795412120186. PubMed DOI

Petrusek A, Hobæk A, Nilssen JP, Skage M, Černý M, Brede N, Schwenk K. Taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda). Zool Scr. 2008;37(5):507–19.

Hernández-López A, Rougerie R, Augustin S, Lees DC, Tomov R, Kenis M, Çota E, Kullaj E, Hansson C, Grabenweger G, et al. Host tracking or cryptic adaptation? Phylogeography of Pediobius saulius (Hymenoptera, Eulophidae), a parasitoid of the highly invasive horse-chestnut leafminer. Evol Appl. 2012;5(3):256–69. PubMed PMC

Mardulyn P, Othmezouri N, Mikhailov YE, Pasteels JM. Conflicting mitochondrial and nuclear phylogeographic signals and evolution of host-plant shifts in the boreo-montane leaf beetle Chrysomela lapponica. Mol Phylogenet Evol. 2011;61(3):686–96. PubMed

Dasmahapatra KK, Elias M, Hill RI, Hoffman JI, Mallet J. Mitochondrial DNA barcoding detects some species that are real, and some that are not. Mol Ecol Resour. 2010;10(2):264–273. doi: 10.1111/j.1755-0998.2009.02763.x. PubMed DOI

Gompert Z, Forister ML, Fordyce JA, Nice CC. Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides. Mol Ecol. 2008;17(24):5231–44. PubMed

Linnen CR, Farrell BD. Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera: Diprionidae) sawflies. Evolution. 2007;61(6):1417–38. PubMed

Toews DPL, Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol. 2012;21(16):3907–3930. doi: 10.1111/j.1365-294X.2012.05664.x. PubMed DOI

Song H, Buhay JE, Whiting MF, Crandall KA. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. P Natl Acad Sci USA. 2008;105(36):13486–13491. doi: 10.1073/pnas.0803076105. PubMed DOI PMC

Funk DJ, Omland KE. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst. 2003;34:397–423.

Mckay BD, Zink RM. The causes of mitochondrial DNA gene tree paraphyly in birds. Mol Phylogenet Evol. 2010;54(2):647–50. PubMed

Franco FF, Lavagnini TC, Sene FM, Manfrin MH. Mito-nuclear discordance with evidence of shared ancestral polymorphism and selection in cactophilic species of Drosophila. Biol J Linn Soc. 2015;116(1):197–210. doi: 10.1111/bij.12554. DOI

Pavlova A, Amos JN, Joseph L, Loynes K, Austin JJ, Keogh JS, Stone GN, Nicholls JA, Sunnucks P. Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird. Evolution. 2013;67(12):3412–28. PubMed

Cheviron ZA, Brumfield RT. Migration-selection balance and local adaptation of mitochondrial haplotypes in rufous-collared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution. 2009;63(6):1593–1605. doi: 10.1111/j.1558-5646.2009.00644.x. PubMed DOI

Hurst GDD, Jiggins FM. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond Ser B Biol Sci. 2005;272(1572):1525–34. PubMed PMC

Skage M, Hobæk A, Ruthová S, Keller B, Petrusek A, Seďa J, Spaak P. Intra-specific rDNA-ITS restriction site variation and an improved protocol to distinguish species and hybrids in the Daphnia longispina complex. Hydrobiologia. 2007;594:19–32.

Dlouhá S, Thielsch A, Kraus RHS, Seda J, Schwenk K, Petrusek A. Identifying hybridizing taxa within the Daphnia longispina species complex: a comparison of genetic methods and phenotypic approaches. Hydrobiologia. 2010;643:107–22.

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. doi: 10.1111/j.1471-8286.2005.01218.x. DOI

Montero-Pau J, Gómez A, Muñoz J. Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnol Oceanogr Methods. 2008;6:218–222. doi: 10.4319/lom.2008.6.218. DOI

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.

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.

Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. PubMed PMC

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol. 2013;30(12):2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Thielsch A, Völker E, Kraus RHS, Schwenk K. Discrimination of hybrid classes using cross-species amplification of microsatellite loci: methodological challenges and solutions in Daphnia. Mol Ecol Resour. 2012;12(4):697–705. doi: 10.1111/j.1755-0998.2012.03142.x. PubMed DOI

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–959. PubMed PMC

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI

Earl DA, vonHoldt BM. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4(2):359–361. doi: 10.1007/s12686-011-9548-7. DOI

Vähä JP, Primmer CR. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol. 2006;15(1):63–72. doi: 10.1111/j.1365-294X.2005.02773.x. PubMed 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 5171, Université de Montpellier II, Montpellier (France) 1996–2004.

Stodola J. Detailed taxonomic and clonal structure of the Daphnia longispina species complex on the longitudinal gradient of the Želivka reservoir. MSc. thesis. Prague: Charles University in Prague; 2013.

Sword GA, Senior LB, Gaskin JF, Joern A. Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acrididae). Syst Entomol. 2007;32(3):420–8.

Campbell NJH, Barker SC. The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplus: fivefold tandem repetition of a coding region. Mol Biol Evol. 1999;16(6):732–740. doi: 10.1093/oxfordjournals.molbev.a026158. PubMed DOI

Wallis GP, Cameron-Christie SR, Kennedy HL, Palmer G, Sanders TR, Winter DJ. Interspecific hybridization causes long-term phylogenetic discordance between nuclear and mitochondrial genomes in freshwater fishes. Mol Ecol. 2017;26:3116–3127. doi: 10.1111/mec.14096. PubMed DOI

Schwenk K, Spaak P. Evolutionary and ecological consequences of interspecific hybridization in cladocerans. Experientia. 1995;51(5):465–481. doi: 10.1007/BF02143199. DOI

Taylor DJ, Sprenger HL, Ishida S. Geographic and phylogenetic evidence for dispersed nuclear introgression in a daphniid with sexual propagules. Mol Ecol. 2005;14(2):525–537. doi: 10.1111/j.1365-294X.2005.02415.x. PubMed DOI

Hobæk A, Skage M, Schwenk K. Daphnia galeata × D. longispina hybrids in western Norway. Hydrobiologia. 2004;526(1):55–62.

Taylor DJ, Hebert PDN. Cryptic intercontinental hybridization in Daphnia (Crustacea): the ghost of introductions past. Proc R Soc Lond Ser B Biol Sci. 1993;254(1340):163–168. doi: 10.1098/rspb.1993.0141. DOI

Wolf HG, Mort MA. Interspecific hybridization underlies phenotypic variability in Daphnia populations. Oecologia. 1986;68:507–511. doi: 10.1007/BF00378763. PubMed DOI

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. doi: 10.1016/j.ijpara.2011.11.004. 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(19):4168–78. PubMed

Alric B, Möst M, Domaizon I, Pignol C, Spaak P, Perga ME. Local human pressures influence gene flow in a hybridizing Daphnia species complex. J Evol Biol. 2016;29(4):720–735. doi: 10.1111/jeb.12820. PubMed DOI

Keller B, Wolinska J, Tellenbach C, Spaak P. Reproductive isolation keeps hybridizing Daphnia species distinct. Limnol Oceanogr. 2007;52(3):984–991. doi: 10.4319/lo.2007.52.3.0984. DOI

Jankowski T, Straile D. Comparison of egg-bank and long-term plankton dynamics of two Daphnia species, D. hyalina and D. galeata: potentials and limits of reconstruction. Limnol Oceanogr. 2003;48(5):1948–55.

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(12):4758–63. PubMed PMC

Rellstab C, Keller B, Girardclos S, Anselmetti FS, Spaak P. Anthropogenic eutrophication shapes the past and present taxonomic composition of hybridizing Daphnia in unproductive lakes. Limnol Oceanogr. 2011;56(1):292–302. doi: 10.4319/lo.2011.56.1.0292. DOI

Marková S, Dufresne F, Manca M, Kotlik P. Mitochondrial capture misleads about ecological speciation in the Daphnia pulex complex. PLoS One. 2013;8(7):e69497. PubMed PMC

Dyer KA, Burke C, Jaenike J. Wolbachia-mediated persistence of mtDNA from a potentially extinct species. Mol Ecol. 2011;20(13):2805–2817. doi: 10.1111/j.1365-294X.2011.05128.x. PubMed DOI

Irwin DE. Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypic clustering. Am Nat. 2012;180(1):35–49. PubMed

Brede N. The reconstruction of evolutionary patterns from Daphnia resting egg banks. Ph.D. thesis. Frankfurtam Main: Goethe University; 2008.

Irwin DE. Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypicclustering. Am Nat. 2012;180(1):35–49. PubMed

Fitzsimmons JM, Innes DJ. No evidence of Wolbachia among Great Lakes area populations of Daphnia pulex (Crustacea : Cladocera). J Plankton Res. 2005;27(1):121–4.

Ebert D. Host-parasite coevolution: insights from the Daphnia-parasite model system. Curr Opin Microbiol. 2008;11(3):290–301. doi: 10.1016/j.mib.2008.05.012. PubMed DOI

Wolinska J, Gießler S, Koerner H. Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Appl Environ Microbiol. 2009;75(22):7051–7059. doi: 10.1128/AEM.01306-09. PubMed DOI PMC

Navia D, Mendonca RS, Ferragut F, Miranda LC, Trincado RC, Michaux J, Navajas M. Cryptic diversity in Brevipalpus mites (Tenuipalpidae). Zool Scr. 2013;42(4):406–26.

Lajus D, Sukhikh N, Alekseev V. Cryptic or pseudocryptic: can morphological methods inform copepodtaxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex. Ecol Evol.2015;5(12):2374–85. PubMed PMC

Navia D, Mendonca RS, Ferragut F, Miranda LC, Trincado RC, Michaux J, Navajas M. Cryptic diversity inBrevipalpus mites (Tenuipalpidae). Zool Scr. 2013;42(4):406–26.

Popova EV, Petrusek A, Kořínek V, Mergeay J, Bekker EI, Karabanov DP, Galimov YR, Neretina TV, Taylor DJ, Kotov AA. Revision of the Old World Daphnia (Ctenodaphnia) similis group (Cladocera: Daphniidae). Zootaxa. 2016;4161(1):1–40. PubMed

Popova EV, Petrusek A, Kořínek V, Mergeay J, Bekker EI, Karabanov DP, Galimov YR, Neretina TV,Taylor DJ, Kotov AA. Revision of the Old World Daphnia (Ctenodaphnia) similis group (Cladocera: Daphniidae).Zootaxa. 2016;4161(1):1–40. PubMed

Zobrazit více v PubMed

Dryad
10.5061/dryad.6jd34