Genetic data has become an essential part of ecological studies, because the analyses of diversity within and among natural populations may grant access to previously overlooked ecological and evolutionary causalities, especially among cryptic species. Here, we present an example of how phylogenetic analysis of molecular data obtained within a DNA barcoding study, in combination with morphological and ecological data from the field and laboratory experiments, unraveled a striking predator-prey interaction between aquatic organisms. The "crown of thorns," a conspicuous morphological feature among water fleas of the Daphnia atkinsoni species complex (Crustacea: Cladocera), is considered to represent a species-specific trait. However, our study, initiated by the analysis of sequence variation in 2 mitochondrial genes, shows that this feature is phenotypically plastic and is induced by chemical cues released by Triops cancriformis, the tadpole shrimp (Notostraca). The trait acts as an effective antipredator defense, and is found in several Daphnia lineages coexisting with notostracans. These facts suggest that the "crown of thorns" evolved in coexistence with this ancient predator group.

Department of Ecology Faculty of Science Charles University Vinicná 7 CZ 12844 Prague Czech Republic

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Tollrian R, Harvell CD. The Ecology and Evolution of Inducible Defenses. Princeton: Princeton Univ Press; 1999.

Tollrian R, Dodson SI. In: The Ecology and Evolution of Inducible Defenses. Tollrian R, Harvell CD, editors. Princeton: Princeton Univ Press; 1999. pp. 177–202.

Alonso M. Crustacea, Branchiopoda. In: Ramos MA, et al., editors. Fauna Iberica. Vol 7. Madrid: Museo Nacional de Ciencias Naturales – Consejo Superior de Investigaciones Científicas; 1996. p. 486. in Spanish.

Benzie JAH. Cladocera: The genus Daphnia (including Daphniopsis) Ghent, Leiden: Kenobi Productions, Backhuys Publishers; 2005. p. 376.

Alonso M. Nota sobre algunes Ctenodaphnia de la Península Ibèrica [Note on some Ctenodaphnia of the Iberian Peninsula] Butl Inst Catalana Hist Nat. 1980;45:47–53. Sec. Zool., 3. in Catalan.

Kelber K-P. New Triopsids (Crustacea, Notostraca) from the Upper Triassic of Frankonia, Germany. Hallesches Jb Geowiss B, Beih. 1998;5:85–86.

Christoffersen K. Predation on Daphnia pulex by Lepidurus arcticus. Hydrobiologia. 2001;442:223–229.

Yee SH, Willig MR, Moorhead DL. Tadpole shrimp structure macroinvertebrate communities in playa lake microcosms. Hydrobiologia. 2005;541:139–148.

Hebert PDN, Ratnasingham S, deWaard JR. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci. 2003;270:S96–S99. PubMed PMC

Moritz C, Cicero C. DNA barcoding: Promise and pitfalls. PLoS Biol. 2004;2:1529–1531. PubMed PMC

Will KW, Mishler BD, Wheeler QD. The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol. 2005;54:844–851. PubMed

Miller SE. DNA barcoding and the renaissance of taxonomy. Proc Natl Acad Sci USA. 2007;104:4775–4776. PubMed PMC

Adamowicz SJ, Colbourne JK, Witt JDS, Hebert PDN. The scale of divergence: A phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus. Mol Phylogenet Evol. 2008 in press. PubMed

Colbourne JK, Hebert PDN. The systematics of North American Daphnia (Crustacea: Anomopoda): A molecular phylogenetic approach. Philos Trans R Soc Lond B Biol Sci. 1996;351:349–360. PubMed

Wesenberg-Lund C. Gronlads Ferskvandsentomostraca. I. Phyllopoda branchiopoda et cladocera. [Freshwater Entomostraca of Greenland. I. Phyllopoda branchiopoda and cladocera.] Vidensk Medd naturhist Foren Kjobenhavn. 1895;56:82–173.

Sars GO. The fresh-water Entomostraca of Cape Province. Ann S Afr Mus. 1916;15:303–351.

Williams DD. Environmental constraints in temporary fresh waters and their consequences for the insect fauna. J N Am Benthol Soc. 1996;15:634–650.

Kerfoot WC, Lynch M. In: Predation: Direct and indirect impacts on aquatic communities. Kerfoot WC, Sih A, editors. Hanover: Univ Press of New England; 1987. pp. 367–378.

Maffi M. Triops granarius (Lucas) (Crustacea) as a natural enemy of mosquito larvae. Nature. 1962;195:722. PubMed

Kumar R, Hwang JS. Larvicidal efficiency of aquatic predators: A perspective for mosquito biocontrol. Zool Stud. 2006;45:447–466.

Boix D, Sala J, Gascon S, Brucet S. Predation in a temporary pond with special attention to the trophic role of Triops cancriformis (Crustacea: Branchiopoda: Notostraca) Hydrobiologia. 2006;571:341–353.

Boix D, Sala J, Moreno-Amich R. Population dynamics of Triops cancriformis (Crustacea: Branchiopoda: Notostraca) of the Espolla temporary pond in the northeastern Iberian peninsula. Hydrobiologia. 2002;486:175–183.

Laforsch C, Ngwa W, Grill W, Tollrian R. An acoustic microscopy technique reveals hidden morphological defenses in Daphnia. Proc Natl Acad Sci USA. 2004;101:15911–15914. PubMed PMC

Dodson SI. Predation of Heterocope septentrionalis on two species of Daphnia: Morphological defenses and their cost. Ecology. 1984;65:1249–1257.

Caramujo M-J, Boavida M-J. Induction and costs of tail spine elongation in Daphnia hyalina x galeata: Reduction of susceptibility to copepod predation. Freshwater Biol. 2000;45:413–423.

Schwenk K, Posada D, Hebert PDN. Molecular systematics of European Hyalodaphnia: The role of contemporary hybridization in ancient species. Proc R Soc Lond B Biol Sci. 2000;267:1833–1842. PubMed PMC

Taylor DJ, Hebert PDN, Colbourne JK. Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation. Mol Phylogenet Evol. 1996;5:495–510. PubMed

Colbourne JK, Wilson CC, Hebert PDN. The systematics of Australian Daphnia and Daphniopsis (Crustacea: Cladocera): A shared phylogenetic history transformed by habitat-specific rates of evolution. Biol J Linn Soc. 2006;89:469–488.

Schwenk K, et al. Genetic markers, genealogies and biogeographic patterns in the cladocera. Aquat Ecol. 1998;32:37–51.

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. PubMed PMC

Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24:1596–1599. PubMed

Farris JS, Kallersjo M, Kluge AG, Bult C. Constructing a significance test for incongruence. Syst Biol. 1995;44:570–572.

Posada D, Crandall KA. MODELTEST: Testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. PubMed

Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Sunderland: Sinauer Associates; 2002.

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. PubMed

Jeschke JM, Tollrian R. Density-dependent effects of prey defences. Oecologia. 2000;123:391–396. PubMed

Agrawal AA, Laforsch C, Tollrian R. Transgenerational induction of defences in animals and plants. Nature. 1999;401:60–63.

Sokal RR, Rohlf FJ. Biometry. 3rd Ed. New York: Freeman; 1995. p. 887.