A New Species in the Daphnia Curvirostris (Crustacea: Cladocera)
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JOURNAL OF PLANKTON RESEARCH VOLUME 28 NUMBER 11 PAGES 1067–1079 2006 j j j j A new species in the Daphnia curvirostris (Crustacea: Cladocera) complex from the eastern Palearctic with molecular phylogenetic evidence for the independent origin of neckteeth ALEXEY A. KOTOV1*, SEIJI ISHIDA2 AND DEREK J. TAYLOR2 1 2 A. N. SEVERTSOV INSTITUTE OF ECOLOGY AND EVOLUTION, LENINSKY PROSPECT 33, MOSCOW 119071, RUSSIA AND DEPARTMENT OF BIOLOGICAL SCIENCES, UNIVERSITY AT BUFFALO, THE STATE UNIVERSITY OF NEW YORK, BUFFALO, NY 14260, USA *CORRESPONDING AUTHOR: [email protected] Received February 22, 2006; accepted in principle June 22, 2006; accepted for publication August 31, 2006; published online September 8, 2006 Communicating editor: K.J. Flynn Little is known of the biology and diversity of the environmental model genus Daphnia beyond the Nearctic and western Palearctic. Here, we describe Daphnia sinevi sp. nov., a species superficially similar to Daphnia curvirostris Eylmann, 1878, from the Far East of Russia. We estimated its phylogenetic position in the subgenus Daphnia s. str. with a rapidly evolving mitochondrial protein coding gene [NADH-2 (ND2)] and a nuclear protein-coding gene [heat shock protein 90 (HSP90)]. Daphnia curvirostris, D. sinevi sp. nov., Daphnia tanakai and D. sp. from Ootori- Ike, Japan, (which, probably, is D. morsei Ishikawa, 1895) formed a monophyletic clade modestly supported by ND2 and strongly supported by HSP90. Our results provide evidence of hidden species diversity in eastern Palearctic Daphnia, independent origins of defensive neckteeth and phylogenetic informativeness of nuclear protein-coding genes for zooplankton genera. INTRODUCTION morphological and genetic approach, Ishida et al. (Ishida Biogeographic and phylogeographic studies have revealed et al., 2006) provided evidence that populations of a Daphnia pronounced regionalism in freshwater zooplankton that is curvirostris-like species from the Hida Mountains in Japan often associated with glacial or orogenic vicariance (Haney belonged to a separate divergent species (Daphnia tanakai and Taylor, 2003). Still, the diversity and biology of fresh- Ishida, Kotov et Taylor, 2006). The results suggested that water zooplankton is poorly understood outside of the further geographic sampling in the eastern Palearctic with Nearctic and western Palearctic (Benzie, 2005). In the east- a combined morphological and genetical assessment of the ern Palearctic, for example, there is marked disagreement diversity might reveal new lineages. about the diversity of the zooplankton model genus Daphnia Daphnia curvirostris-like species possess a mixture of sev- O. F. Mu¨ller, 1785 (Crustacea: Cladocera). Glagolev eral diagnostic morphological features from the com- (Glagolev, 1995) reported no endemic eastern Russian monly recognized subgenera of Daphnia. As such, an species or lineages, despite the existence of well-established understanding of the diversity and evolution of this glacial refugia. Ishikawa (Ishikawa, 1895a, 1895b, 1896) anomalous group is critical for understanding morpho- and Ue´no (Ue´no, 1972), however, described several ende- logical innovations and adaptative radiation of the entire mic Daphnia species from Japan. Using a combined genus Daphnia. For example, the functional significance doi:10.1093/plankt/fbl041, available online at www.plankt.oxfordjournals.org Ó The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH VOLUME 28 NUMBER 11 PAGES 1067–1079 2006 j j j j of the subgenera-defining second pecten on the postab- curvirostris complex, Daphnia sinevi sp. nov. and (iii) assess dominal claw is unknown. Ishida et al.’s (Ishida et al., the number of evolutionary origins of neckteeth in 2006) evidence that a curvirostris-like species can possess Daphnia. the extreme phenotypes from a row of fine setules (long- ispina type) to a group of strong teeth (pulex type) makes D. tanakai a valuable subject to understand the functional METHOD significance of the pecten. Unfortunately, despite the mtDNA sequence analysis of Ishida et al. (Ishida et al., Genetic analyses were performed using the sequences of 2006), the phylogenetic position of D. tanakai within a nuclear protein-coding gene [heat shock protein 90 Daphnia remains unresolved. (HSP90)] and a mitochondrial protein-coding gene In a survey of 80 samples from the Far East of Russia [NADH-2 (ND2)] for D. sinevi sp. nov. and 16 other (Primorski Krai, Khabarovsk Area and Sakhalin Area), species of Daphnia including an undescribed species we found a curvirostris-like population (Fig. 1) with yet from Ootori-Ike (Table I). The ND2 sequences of seven another suite of mixed morphological characters. The species were obtained from GenBank (DQ132610, specimens possessed neckteeth, defensive structures pre- DQ132613–DQ132620 and DQ132627). Multiple spe- viously recorded from species closely related to Daphnia cimens (2–10) of each curvirostris-like species (D. curvirostris, pulex and to Daphnia dentifera but unrecorded from D. D. tanakai, D. sinevi and D. sp.) were used for sequence curvirostris-like specimens (Benzie, 2005). This structure, analyses. We extracted genomic DNA using which generally appears in the smaller instars, is believed QuickExtract (Epicentre) as described in Ishida et al. to be a low-cost adaptation against invertebrate preda- (Ishida et al., 2006). Each 50 mL PCR reaction consisted tion (Tollrian, 1995; Colbourne et al., 1997). Beaton and of 5 mL of extracted DNA, 10 PCR buffer [50 mM Â Hebert (Beaton and Hebert, 1997) found that polyploid KCl, 1.5 mg MgCl2, 10 mM Tris–HCl pH 8.3, 0.01% nuclei were associated with the region of necktooth (w/v) gelatin], 2 mM each dNTPs, 1 mM each primer growth and suggested that a common developmental and 1 U of Taq DNA polymerase. The primers and the mechanism may be present in the distantly related PCR thermal cycling parameters for the mitochondrial Daphnia that express neckteeth. ND2 gene ( 1000 bp) were described in Ishida et al. Here, we aimed to (i) address the phylogenetic posi- (Ishida et al., 2006). We initially used the degenerate tions of D. curvirostris-like specimens from the eastern HSP90 primers (listed as hsp82) of Welch and Meselsen Palearctic by using both nuclear and mtDNA protein- (Welch and Meselsen, 2000) and obtained an 760 bp coding genes, (ii) describe a new species from the PCR product from Daphnia dubia, Daphnia laevi s and Daphnia magna. Cloning was performed for these PCR products using the TOPO TA Cloning Kit (Invitrogen), and the colonies were sequenced. We then developed specific primers for Daphnia ( 700 bp fragment of HSP90 with two introns): 50-TTACGAGTCCA- GATGGGCTT-30 and 50-ATCCGTTATGAATCC- CTGACTGA-30. PCR thermal cycling parameters for these specific primers were 40 cycles of 948C for 30 s, 508C for 30 s and 728C for 1 min with Peltier thermal cycler (Bio-Rad). The HSP90 PCR products of Daphnia pulicaria possessed numerous sequence ambiguities and were cloned before sequencing. Direct sequencing was performed for the other HSP90 PCR products. Sequencing was performed by Genaissance Pharmaceuticals (New Haven, USA) or the Roswell Park Cancer Institute (Buffalo, USA). Intron boundaries of the HSP90 sequences were iden- tified by comparing arthropod HSP90 mRNA sequences (e.g. AY528900 and AY423488) and by examining intron-splicing signature sequences. The HSP90 exon sequences (621 bp) and the ND2 sequences (962 bp) Fig. 1. A map of localities in Japan and the Far East of Russia, where were aligned manually. These nucleotide alignments Daphnia curvirostris-like species were collected for this study. were used for neighbor joining (NJ), maximum 1068 Table I: Daphnia specimens subjected to DNA sequencing Taxon Sampled location Latitude Longitude Number of Gene accession number specimens HSP ND2 HSP ND2 Daphnia sinevi sp. nov. Avangard, Nakhodka Area, 428480N 1328530E 3 2 DQ845251 DQ845269 A. A. Primorski Krai, Russia KOTOV, Daphnia sp. Ootori-Ike, Yamagata, Japan 388220N 1398500E 2 4 DQ845252 DQ845270 Daphnia tanakai Ishida, Kotov et Taylor, 2006 Kagami-ike (K), Gifu, Japan 368200N 1378360E 1 5 DQ845253 DQ132618 Daphnia tanakai Ishida, Kotov et Taylor, 2006 Midori-ga-ike (M-1), Toyama, Japan 368350N 1378360E 1 4 DQ845254 DQ132616 S. ISHIDA Daphnia tanakai Ishida, Kotov et Taylor, 2006 Midori-ga-ike (M-2), Toyama, Japan 368350N 1378360E 0 1 n/a DQ132617 Daphnia curvirostris Eylmann, 1887 Pilgrim Hotspring, AK, USA 65850N 1648550W 3 1 DQ845255 DQ132619 Daphnia curvirostris Eylmann, 1887 Somotor, Southeastern Slovakia 488230N 218490E 0 1 n/a DQ132620 AND Daphnia longispina O. F. Mu¨ ller, 1785 Unnamed pond south of 678370N 238330E 1 1 DQ845256 DQ132610 D. Muono, Lapin Laani, Finland J. TAYLOR 10 Daphnia dentifera Forbes, 1893 Crossman’s Pond, NY, USA 43820N 778280W 1 1 DQ845257 DQ845271 6 9 Daphnia cucullata Sars, 1862 Hancza, Poland 548150N 228480E 1 1 DQ845258 DQ845272 Daphnia galeata Sars, 1864 Ikeda-Ko, Kagoshima, Japan 318140N 1308340E 1 1 DQ845259 DQ845273 j Daphnia laevis Birge, 1897 Cape Cod, MA, USA 42840N 708120W 1 1 DQ845260 DQ132614 NEW Daphnia dubia Herrick, 1883 emend. Pond in the South of Cornerbrook, n/a n/a 1 1 DQ845261 DQ132615 Herrick, 1885 Newfoundland, Canada SPECIES Daphnia cristata Sars, 1862 Puruvesi, Ita-Suomen Laani, Finland 618460N 298210E 1 1 DQ845262 DQ132613 Daphnia longiremis Sars, 1861 Deer Lake, Newfoundland, Canada 498110N 578270W 1 1 DQ845263 DQ845274 OF Daphnia pulicaria Forbes, 1893 Honeoye Lake, NY, USA 428450N 778310W 1 1 DQ845264 DQ845275 D Daphnia ambigua Scourfield, 1947 Fresh Pond, MA, USA 418410N 70890W 1 1 DQ845265 DQ845276 A P H Daphnia ephemeralis Schwartz et Pond in Amherst, NY, USA 43820N 788470W 1 1 DQ845266 DQ845277 N I Hebert, 1985 A Daphnia lumholtzi Sars, 1885 Burn Lake, NM, USA 328180N 1068480W 1 1 DQ845267 DQ845278 Daphnia magna Straus, 1820 Clone from WARD’S n/a n/a 1 1 DQ845268 DQ132627 Natural Science, USA HSP90, heat shock protein 90; ND2, NADH-2. The columns of HSP90 and ND2 indicate the number of specimens used for the phylogenies of each gene.