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Home , Ctenopoda, Endorheic basin, Leptodora, Polyphemus (crustacean)

Journal of Biogeography (J. Biogeogr.) (2011) 38, 359–370

ORIGINAL Biogeography and evolution of the ARTICLE Holarctic zooplankton (Crustacea: : Haplopoda) Lei Xu1, Bo-Ping Han1*, Kay Van Damme2, Andy Vierstraete2, Jacques R. Vanfleteren2 and Henri J. Dumont2*

1Institute of Hydrobiology, Jinan University, ABSTRACT Guangzhou 510632, , 2Department of Aim To reconstruct the phylogeographic history of the Holarctic carnivorous Biology, Ghent University, B-9000 Ghent, Belgium genus Leptodora (Crustacea: : Haplopoda). Location We studied the DNA of between one and five specimens each from 28 populations distributed across the Holarctic, but with emphasis on . Methods We sequenced a mitochondrial (cytochrome c oxidase subunit I) and a nuclear (elongation factor-1a) gene, and combined this molecular information with geological and palaeoclimatological data. Haplotype networks and phylogenetic trees were constructed using a Bayesian and maximum likelihood approach. A molecular clock was applied. Results Leptodora consists of three clades (Leptodora kindtii in , Leptodora richardi in China and Japan, and Leptodora sp. in ), with insular subclades in Japan and in the eastern Mediterranean. The North American clade was not studied in detail. Leptodora richardi is the more thermophilic of the three. It extends from the Tropic of Cancer in the south to the Heilong Basin in the north. The western European L. kindtii is more cold-water adapted than the eastern Mediterranean subclade. ‘West European’ and ‘Chinese’ clades are broadly separated by a hybrid zone in and as far west as the . These hybrids have the mitochondrial DNA of L. kindtii, the nuclear DNA of L. richardi and the low-temperature preference of L. kindtii, and may have formed as recently as the Holocene hypsithermal. A pure L. kindtii population in the Upper catchment, east of the Dzungarian Gates, has been sequestered in endorheic Wulungu, , since the mid-Pleistocene. Main conclusions Application of a molecular clock places the most recent common ancestor of the North American, East Asian and European populations in the mid-. The North American taxon is still living in isolation, while the Eurasian taxa, separated by the Alpine folding, made contact again in the Pleistocene, when the cold-stenothermic L. kindtii repeatedly moved eastwards across Siberia and back. The population in Xinjiang is a relict of an early wave coming from : it crossed the Dzungarian Gates during a humid mid-Pleistocene event, probably corresponding to the Apsheron transgression in the Caspian Basin. Later aridity isolated it there, and it started accumulating *Correspondence: Bo-Ping Han, Institute of private haplotypes. The Holocene Euro-Siberian hybrid zone may eventually Hydrobiology, Jinan University, Guangzhou engulf all European populations. 510632, People’s Republic of China and Henri J. Dumont, Department of Biology, Ghent Keywords University, B-9000 Ghent, Belgium. Apsheron humid phase, Cladocera, Dzungarian Gates, Eurasia, haplotype E-mails: [email protected]; [email protected] networks, hybridization, Leptodora, molecular phylogeny.

ª 2010 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 359 doi:10.1111/j.1365-2699.2010.02409.x L. Xu et al.

all but the northern extreme of two of Europe’s three main INTRODUCTION glacial refugia (Willis & Whittaker, 2000; Sommer & Zachos, The zoogeography of freshwater zooplankton, and particularly 2009). In contrast, it is not uncommon in piedmont in of the four orders of the Cladocera (water fleas) (Crustacea: the , , and in Mediterranean (). Branchiopoda), has been a fertile field of research for the past This reveals a different thermal behaviour between the western 30 years. In a first phase, the old theory of cosmopolitanism (more cold adapted) and eastern (more warm adapted, limit of was refuted: some groups were found to be mainly temperate southern extent c.37 N) populations in Europe and in distribution (e.g. the daphniids), others tropical (e.g. the Minor. Further east, Leptodora is absent from (Lo¨ffler, sidids) (see Dumont & Negrea, 2002, for an overview). More 1961) and rare in mountainous and arid . In recently, detailed morphological and molecular studies have , for example, it is known from the north, namely started refining these results. Usually, a considerable amount of the Irtysh catchment (see below) and , the cryptic diversity is revealed, for example in the ctenopod genus endpoint of the Ili River, but it is absent from arid (Rowe et al., 2007) and in the onychopod genus Turkmenistan and from most of . In (Xu et al., 2009). In addition, well-defined (H.J.D., pers. obs.) it is lacking from the saline west and dry patterns of distribution emerge within the Holarctic. south. It is locally common in eastern Mongolia, but only in Here, we study the Holarctic genus Leptodora Lilljeborg, the upper catchment of the Heilong River, where probably 1861, noteworthy because of the large size of individuals (up to L. richardi or a hybrid kindtii · richardi occurs (see below). 15 mm), and because it is the sole extant representative of the On islands it is known from Britain, including Ireland, and the order Haplopoda. We explore whether it is genetically Japanese islands of Hokkaido and Honshu (see Table 1 for homogeneous across its geographic range rich in topographic material examined, the latter again L. richardi). In China, and climatic barriers and, if not, what geological and L. richardi occurs in the northern provinces of Xinjiang, Inner palaeoclimatic events may have shaped its phylogeny. Mongolia, and Heilongjiang; south and east it is found as far as Leptodora had remained monotypic, with Leptodora kindtii Guangdong Province (Jiang & Du, 1979), where it narrowly (Focke, 1844) the only recognized , until Korovchinsky crosses the Tropic of Cancer, making it the most thermophilic (2009) described Leptodora richardi from the Heilong (Chinese of all Leptodora species (limit of southern extent 21 N, of name)–Amur (Russian name) Basin between the Russian Far northern extent 45 N). East and China. Leptodora richardi (H.J.D., pers. obs.) is From to eastern Siberia, Leptodora rarely widespread in Japan, Korea and China. Mountain chains, penetrates the zone, but in the valleys of the , hydrogeographic discontinuities and saline and marine envi- and Anadyr , a taxon that is clearly more cold- ronments are biogeographic barriers for Leptodora. It is seldom adapted than L. richardi extends north to 68 N (N. M. observed in river , but upon reservoir construction it Korovchinsky, Russian Academy of Sciences, Moscow, pers. is among the first colonizers of the newly created water bodies. comm.; Korovchinsky & Boikova, 2008; Korovchinsky, 2009). Its resting stages (encysted gastrulae enveloped in a layer of Finally, the genus is absent from Iceland (A. Einarsson, jelly) therefore seem able to maintain themselves across the Myvatn, Iceland, pers. comm.) and Greenland (Hrbacek et al., entire length of major rivers. Downstream migration may be 1978). simply by gravity, and upstream migration by phoretic means, Leptodora is also widespread in the USA (Dodson & Frey, on or inside vertebrates, the prime candidates being migratory 2001) and in Canada (Patalas et al., 1994). Detailed distribu- waterbirds (Proctor, 1964; Proctor & Malone, 1965; Charal- tional data for within the USA are not available, but it seems to ambidou & Santamarı´a, 2002; De Meester et al., 2002; Green be lacking from the north of Alaska, Yukon and north-east and et al., 2002; Havel & Shurin, 2004). . Southernmost records in the USA are in The preferred habitat of adults of this zooplanktivorous Oklahoma, southern Texas (Holt et al., 1978), Arkansas, is stagnant water, ranging from medium-sized ponds to Missouri, Louisiana and other southern states (Rickett & big lakes. The type locality is an artificial city-ditch with Watson, 1994) but do not reach (M. Elı´as-Gutie´rrez, eutrophic water in Bremen, Germany (Dumont & Hollwedel, Ecosur, Mexico, pers. comm.). These deserve more 2009), but at the other end of the scale it is also found in huge taxonomic and ecological study; the fact that they extend oligotrophic lakes, such as Lake Leman (see Table 1 for a list of between 30 and 70 N suggests that several North American material examined), usually below 600 m a.s.l. taxa, differing in thermal preferences, may exist. On the whole, No analysis using information from the genome (DNA) has Leptodora emerges as a Holarctic taxon with a preference for a so far addressed possible subdivisions within Leptodora, their temperate climate, avoiding the extreme cold of the Arctic and origin and geographic range. The type locality of L. kindtii is of high mountain lakes (only Behning, 1941, cites Leptodora situated in the European part of what so far appears to be a from lakes in the , up to 2000 m a.s.l.), but also the biogeographic continuum from central France across the heat of large parts of the Mediterranean zone. The genus only Russian and Siberian Plains to the hilly Russian and reaches as far south as the subtropics in south-east China. China. In the south-west, the species does not reach the foot of There is a puzzling presence of a population of Leptodora in the Pyrenees, and is absent from the Iberian Peninsula, North the Kashmir , in lakes at about 1500 m a.s.l. (Brehm, and south of c.45 N. It is therefore lacking from 1936; Michael & Sharma, 1988). This record invites closer

360 Journal of Biogeography 38, 359–370 ª 2010 Blackwell Publishing Ltd Biogeography and evolution of Leptodora

Table 1 List of populations of Leptodora examined, with location, coordinates, haplotypes identified, GenBank accession numbers and name of collector(s).

GenBank accession numbers Location Latitude and COI COI EF1a Code (state/lake or ) longitude haplotype clade haplotype COI EF1a Collectors

Germany Bremen city Ditches 5304¢30¢¢ N H1 H2 A1 h1 HM802808 HM802852 G. Brandorff Ger 848¢25¢¢ E HM802809 HM802853 B. Scharf, W. Hollwedel HM802810 Poland Lake Mikolajki 5347¢32¢¢ N H3 H7 A1 h4 HM802798 HM802858 J.Ejsmont-Karabin Pol 1915¢04¢¢ E HM802799 HM802859 Holland Biesbos area 5149¢20¢¢ N H4 H5 A1 h4 HM802803 HM802846 H.A.M. Ketelaars Hol 439¢07¢¢ E HM802804 HM802847 HM802805 Belgium Lake Donk 5103¢14¢¢ N H4 H5 A1 h6 HM802806 HM802850 H.J. Dumont Bel 357¢20¢¢ E HM802807 HM802851 Romania Rom Bicaz Reservoir 4656¢44¢¢ N H6 A1 h4 HM802792 HM802860 I. Miron 2608¢19¢¢ E HM802793 HM802861 HM802794 Ireland Lake Derg 5258¢30¢¢ N H8 H9 H10 A1 h4 HM802789 HM802856 A. Pociecha IreD 819¢30¢¢ W HM802790 HM802857 HM802791 Lake Balaton 4649¢49¢¢ N H11 A1 h4 HM802786 HM802854 J. Padisak Hun 1744¢03¢¢ E HM802787 HM802855 HM802788 Neusiedler see 4758¢37¢¢ N H11 A1 h2 h3 HM802783 HM802848 A. Herzig Aus 1650¢41¢¢ E HM802784 HM802849 HM802785 France Lake Leman 4758¢37¢¢ N H12 H13 A1 h8 h9 HM802795 HM802844 O. Anneville Fra 1650¢41¢¢ E HM802796 HM802845 HM802797 Slovenia Podpesko Lake 4602¢25¢¢ N H14 H15 A1 h10 h11 HM802800 HM802862 A. Brancelj Slo Ljubljana area 1450¢48¢¢ E HM802801 HM802863 HM802802 Russia Ryazan area 5438¢03¢¢ N H16 A1 h18 HM802819 HM802871 A. Kotov RusRya 3944¢20¢¢ E HM802820 HM802872 HM802821 RusKha Khabarovsk area 4838¢51¢¢ N H16 A1 h14 h15 HM802822 HM802866 A. Kotov 13505¢16¢¢ E HM802823 HM802867 HM802824 RusTom Tomsk area 5627¢50¢¢ N H17 A1 h19 HM802812 HM802873 A. Kotov 8457¢45¢¢ E RusNov Novosibirsk area 5502¢26¢¢ N H16 H19 A1 h12 HM802816 HM802869 A. Kotov 8255¢49¢¢ E H20 HM802817 HM802818 RusTve Tver area 5651¢18¢¢ N H18 H22 A1 h12 HM802813 HM802874 A. Kotov 3555¢31¢¢ E HM802814 RusPsk Pskov area 5750¢41¢¢ N H21 A1 h7 HM802815 HM802870 A. Kotov 2818¢03¢¢ E RusMosc Moscow area 5545¢12¢¢ N H23 A1 h20 HM802811 HM802868 A. Kotov Glubokoe Lake 3738¢21¢¢ E RusAst Volga River at 4621¢17¢¢ N – – h23 – HM802877 V. Alekseev Astrakhan 4803¢10¢¢ E Turkey Catalan dam (Adana) 3704¢01¢¢ N H28 A2 h4 HM802780 HM802864 S. Karaytug Tur 3523¢40¢¢ E HM802781 HM802865 HM802782 USA Lake Mendota 4306¢04¢¢ N H29 C h21 h22 HM802763 HM802830 S.I. Dodson US 8925¢43¢¢ W HM802764 HM802831

Journal of Biogeography 38, 359–370 361 ª 2010 Blackwell Publishing Ltd L. Xu et al.

Table 1 Continued

GenBank accession numbers Location Latitude and COI EF1a Code (state/lake or region) longitude haplotype COI clade haplotype COI EF1a Collectors

China Lake Wulungu 4724¢01¢¢ N H24 H25 A1 h5 HM802825 HM802875 Bo-Ping Han ChiWu 8745¢29¢¢ E H26 H27 HM802826 HM802876 HM802827 HM802828 HM802829 ChiFe Fei Laixia reservoir 2344¢05¢¢ N H30 H34 B1 h12 HM802770 HM802835 Bo-Ping Han 11301¢04¢¢ E HM802771 HM802836 HM802772 ChiQ Qian Daohu 2932¢30¢¢ N H31 B1 h12 HM802767 HM802839 Bo-Ping Han reservoir 11856¢42¢¢ E HM802768 HM802840 HM802769 ChiXin Xin Licheng area 4340¢16¢¢ N H32 B1 h13 HM802776 HM802841 Bo-Ping Han 12522¢57¢¢ E ChiLiu Liu Xihe reservoir 2345¢23¢¢ N H33 B1 h12 HM802773 HM802837 Bo-Ping Han 11346¢04¢¢ E HM802774 HM802838 HM802775 ChiXu Xu Jiahe reservoir 3133¢11¢¢ N H30 B1 h2 HM802765 HM802842 Lei Xu 11337¢04¢¢ E HM802766 HM802843 Japan Lake Biwa 3520¢47¢¢ N H35 H36 H37 B2 h17 HM802777 HM802833 M. J. Grygier Jap 13610¢12¢¢ E HM802778 HM802834 HM802779 Canada Lake 4513¢42¢¢ N – – h16 – HM802832 B. Beisner Can Memphre´magog 7212¢08¢¢ W

COI, cytochrome c oxidase subunit I; EF1a, elongation factor-1a.

study, because it is situated south of the great dividing chain of ethanol, rinsed with double-distilled (dd) H2O, transferred mountains of Eurasia (see Discussion), which Leptodora does individually to a reaction tube and stored on ice. Next, we not normally cross. The local population may therefore added 200 lL of warm cell lysis solution and 3 lLof ) represent an old relict, pre-dating even the alpine folding, or proteinase K (20 mg mL 1). We vortexed and subsequently a recent invader, brought by migratory waterfowl from Siberia, incubated the mixture for 2 h at 65 C and then for 2–3 days great numbers of which spend the winter in the at 55 C with daily addition of 2 lL of fresh proteinase K. north-west of Srinagar. Next, we added 100 lL of Precipitation Solution, vortexed vigorously at an intermediate speed for 20 s and put it on ice for 2 min, then centrifuged at 19,000 g for 10 min at room MATERIALS AND METHODS temperature. We carefully removed the supernatant and transferred it to a clean 500 lL microcentrifuge tube Sampling containing 200 lL of isopropanol at room temperature. We Animals were collected in the field using dip plankton nets of centrifuged at 19,000 g for 1 min at room temperature and mesh size 110 lm, and fixed in 70% ethanol. Upon receiving carefully decanted the supernatant. Finally, the pellet was samples (either sent by mail or collected in the field by washed with 70% ethanol, dissolved in 40 lL DNA hydration ourselves, see Table 1 for a list) all specimens were rinsed and solution and stored at )20 C. examined under a dissecting microscope, transferred to a fresh Part of the cytochrome c oxidase subunit I (COI) gene tube and preserved in 95% ethanol at 4 C. (696 bp) was amplified from total genomic DNA using the polymerase chain reaction (PCR). Primers used for PCR were CO1490F (5¢-GGT CAA CAA ATC ATA AAG ATA TTG G-3¢) DNA extraction, PCR amplification and sequencing and CO2198R (5¢-TAA ACT TCA GGG TGA CCA AAA AAT Total genomic DNA was extracted using a genomic DNA CA-3¢) (Folmer et al., 1994). Each 50 lL consisted of 31.25 lL isolation kit (products and protocol from Wizard Genomic dd H2O, 5 lL PCR buffer, 5 lL CoralLoad concentrate,

DNA, Purification Kit type A1225, Promega, Madison, WI, 4 lLof25lm MgCl2,1lLof10lm dinucleotides (dNTPs), USA). We modified the standard protocol as follows: for 0.5 lLof25lm solution of each primer, 2.5 lL of DNA DNA extraction, specimens were picked out from 95% template and 0.25 lL of TopTaq DNA polymerase (Qiagen,

362 Journal of Biogeography 38, 359–370 ª 2010 Blackwell Publishing Ltd Biogeography and evolution of Leptodora

Hilden, Germany). The PCR conditions for amplification were: (Posada & Crandall, 1998, 2001). Analyses were performed 40 cycles set at 30 s at 96 C (denaturation), 30 s at 51 C under unweighted parsimony, maximum likelihood (ML) and (annealing) and 60 s at 72 C (extension), followed by 7 min Bayesian inference. Maximum parsimony (MP) analysis was at 72 C (final-extension) on a 2720 Thermal Cycler (Applied performed in paup* 4.0 beta 10 (Swofford, 2003) with the Biosystems, Foster City, CA, USA). The PCR products were following settings: heuristic search, 100 bootstrap replicates, 10 sequenced on an ABI 3130XL automatic sequencer (Applied random sequence addition replicates and tree bisection– Biosystems). reconnection branch (TBR) swapping. ML analysis, also with For amplification of the elongation factor-1a (EF1a) gene paup*, was with heuristic search, TBR branch swapping, 10 we employed a nested-PCR strategy to eliminate double random sequence addition replicates and 100 bootstrap peaks. We first selected one or two specimens from one replicates. Bayesian analysis was performed using MrBayes, population and amplified their genomic DNA using degen- v.3.1.2 (Huelsenbeck & Ronquist, 2001; Huelsenbeck et al., erate primers M44-1 (GCT GAG CG(C/T)GA(A/G) CGT 2001). The Markov chain Monte Carlo (MCMC) analysis was GGT ATC AC) and rcM53-2 (GCA ATG TG(A/G) GCT run in four parallel chains for 2,000,000 generations, sampling GTG TGG CA) (Cho et al., 1995; Goetze, 2006). We used every 1000 generations. Majority rule consensus trees were touchdown PCR according to the following specifications: reconstructed after discarding the burn-in of 500 and displayed 95 C for 3 min, stage 1 (95 C for 30 s, 58 C for 30 s, with treeview v.1.6.6 (Page, 1996). 72 C for 1 min) for 10 cycles, stage 2 (95 C for 30 s, 58– Distances between COI sequences were calculated using the 48 C for 30 s, 72 C for 1 min) over 20 cycles, decreasing Kimura two-parameter (K2P) substitution model in mega 4.1 the annealing temperature by 0.5 C at each cycle, and stage (Kumar et al., 2008). We used uniform rates, and standard 3 (95 C for 30 s, 48 C for 30 s, 72 C for 1 min) for 5 error estimates were obtained by a neighbour-joining (NJ) cycles. The DNA bands were recovered from agarose gel and bootstrap procedure with 10,000 replicates. To visualize the inserted into a pMD19-T Vector plasmid (TaKaRa, Beijing, genetic diversity among COI and EF1a haplotypes we China) and transfected into Escherichia coli cells. Plasmid constructed a tcs network of haplotypes from the locations DNA was extracted for sequencing after overnight incuba- studied, using tcs v.1.21 (Clement et al., 2000). In the tion. We sequenced multiple clones and identified the inserts resulting maximum parsimony network, we applied the option using Blast searches against GenBank, yielding several EF1a Fix Connection Limit Steps at 100. We tested the possibility reads. We selected those that matched with . that the COI phylogeny is consistent with a molecular clock by Based on this information, we designed the primers EF12F running the programs dnaml and dnamlk on the same (ATT GAC ATT GCT TTG TGG AA) and EF866R (GTA data (Felsenstein, J. http://cmgm.stanford.edu/phylip/dnamlk. GCC ATT GCT GAT TTG AC), between M44-1 and rcM53- html), the program dnamlk running the data under the 2, using Primer Premier version 5.0 (Premier Biosoft Inst., constraint that the resulting tree must be consistent with a Palo Alto, CA, USA), isolating a region of 835 bp of the molecular clock. exon part of the gene. Our collections of samples were thereafter first amplified RESULTS with M44-1 and rcM53-2, using 3 lL of the product of the first amplification as the template, and reamplified with EF12F and Alignments and sequence variation EF866R. The PCR conditions for the second amplification were 40 cycles of 30 s at 95 C, 30 s at 52 C and 60 s at 72 C, We obtained the sequence of the COI gene from 67 individuals followed by 7 min at 72 C. The products of the second of Leptodora from eighteen European populations, seven Asian amplification were sequenced on an ABI 3130XL sequencer. A populations and one North American population, and a complete absence of double peaks in all sequence reads dispels sequence from GenBank (DQ889107). The average base any concern about the occurrence of allelic variance or composition was A = 23.9%, C = 22.1%, G = 21.9%, T = incidental amplification errors. 32.1%, transition/transversion (ti/tv) ratio = 2.5. The partial sequence of the EF1a gene was amplified from 48 individuals from 28 Holarctic populations, also including a Phylogenetic analysis sequence from GenBank (AF526278). The EF1a alignment of The authenticity of all COI and EF1a sequences was verified by 805 bp showed no length variation within populations. The aBlast search in GenBank. The sequences were assembled and average EF1a base composition was A = 23.6%, C = 25.0%, edited in Bioedit (Hall, 1999), and aligned under default G = 29.1%, T = 22.2%, with a ti/tv ratio = 7.1. options. The first 20 and last 10 bp were not included, because they were missing in some sequences. The total length of the Phylogenetic analysis sequenced segments after alignment was 672 bp for COI and 805 bp for EF1a. The best-fitting model selected by MrModeltest 2.3 for the Before phylogenetic analysis, we used MrModeltest v.2.3 COI data set was HKY+G with a relative AIC weight of (Nylander, 2004) to select the best-fit models of nucleotide 0.6998 and gamma distribution shape parameter 0.2538. The substitution under the Akaike information criterion (AIC) sequence data were analysed using MP, ML and Bayesian

Journal of Biogeography 38, 359–370 363 ª 2010 Blackwell Publishing Ltd L. Xu et al. inference. Two sequences of appear in all phylogenetic analyses. Clade A contains two well- (AY075048 and DQ889121) were used as an outgroup. All supported sublineages from the Central European plain to the phylogenetic calculations (Bayesian inference, ML and MP) Dzungarian Basin and Siberian plains (A1) and South Anatolia resulted in trees of similar topology (Figs 1 & 2, ML figure (A2). Clade B also contains two well-supported sublineages not shown). from east of China (B1) and Lake Biwa, Japan (B2). Clades B1 COI reveals three well-supported main clades: these Euro- and B2 are sister groups with high support. Clade C, from North Siberian (A), East Asian (B) and North American (C) clades America, lacks detail because of the limited material examined.

US 1 (a) 1.00 US 2 (b) 0.89 RusRya 1 USNCBI C 0.64 RusRya 2 ChiXin RusMosc ChiO 1 1.00 1.00 ChiO 2 RusAst ChiO 3 RusKha 1 ChiXu 1 ChiXu 2 RusKha 2 ChiFe 1 ChiXin 0.99 0.60 ChiFe 2 B1 ChiFe 3 Jap 1 ChiLiu 1 Jap 2 ChiLiu 2 Can ChiLiu 3 RusTve 1 Jap 2 0.91 Jap 1 RusTom 1.00 Jap 3 B2 RusNov 1 Pol 1 Pol 2 ChiXu 2 Hol 1 ChiXu 1 Hol 2 ChiQ 1 Hol 3 0.93 1.00 Bel 1 ChiQ 2 Bel 2 ChiLiu 2 Ger 1 Aus 1 ChiLiu 1 Aus 2 ChiFe 2 1.00 Aus 3 Hun 1 ChiFe 1 Hun 2 US 1 Hun 3 US 2 0.76 IreD 1 ChiWu 1 IreD 2 IreD 3 ChiWu 2 0.62 Fra 1 Aus 1 Fra 2 Ger 2 Fra 3 Slo 1 Ger 1 Slo 2 Slo 1 Slo 3 Rom 1 A1 Slo 2 0.90 Rom 2 Bel 1 Rom 3 Bel 2 Ger 2 1.00 Ger 3 Fra 1 Rus Nov 3 Fra 2 Rus Rya 1 Rus Rya 2 Hol 1 Rus Rya 3 RusPsk Rus Kha 1 Tur 2 Rus Kha 2 0.99 Rus Kha 3 Tur 1 RusTve 2 Rom 2 RusNov 1 RusNov 2 Rom 1 RusMsco Pol 2 RusPsk Pol 1 RusTom RusTve 1 IreD 2 ChiWu 1 IreD 1 0.91 ChiWu 2 Hun 2 ChiWu 3 ChiWu 4 Hun 1 Ger NCBI ChiWu 5 Tur 1 0.1 Tur 2 Aus 2 Tur 3 A2 0.1 Hol 2

Figure 1 Phylogenetic estimate of the phylogeny of Leptodora based on the sequence of its cytochrome c oxidase subunit I (COI) (a) and elongation factor-1a (EF1a) (b) genes by Bayesian inference. Numbers on the nodes are Bayesian posterior probabilities. The COI-based phylogeny shows three well-supported main branches, identifying a North American (C) clade, an East Asian clade (B1-2) and a North Eurasian clade (A1). Anatolian (A2) and Japanese (B2) subclades are also well supported. The EF1a-based phylogeny identifies a European clade (augmented with ChiWu, the population from Xinjiang), and an Asian–American clade. It classifies all Russian populations (save Pskov in the Baltics) with the ‘Asian’ clade.

Aus 1 53.3 Aus 1 (a)Hun 3 (b) 87.5 Hun 2 Aus 2 Hun 1 85.9 ChiWu 1 Aus 3 ChiWu 2 Aus 2 54.5 63.5 Fra 2 99.5 Slo 1 81.6 Fra 3 Slo 2 Fra 1 60.2 IreD 1 56.0 Bel 1 90.0 IreD 3 Bel 2 IreD 2 Slo 1 Hol 1 76.9 Slo 3 Tur 2 Slo 2 Tur 1 RusMosc 50.9 58.0 RusNov 2 Rom 1 RusNov 1 Rom 2 RusPsk Pol 2 RusTve 2 Pol 1 85.0 RusTom IreD 2 77.0 RusNov 3 RusTve 1 RusKha 3 A1 IreD 1 RusKha 2 Hun 2 RusKha 1 82.7 Hun 1 RusRya 3 61.1 RusRya 2 Ger NCBI RusRya 1 Ger 1 ChiWu 1 Ger 2 89.0 ChiWu 5 Hol 2 ChiWu 4 ChiWu 3 Fra 1 Rom 1ChiWu 2 RusPsk 57.0 Rom 3 Fra 2 Rom 2 86.6 RusKha 1 100.0 Pol 1 85.5 Ger 3 100.0 RusKha 2 Ger 2 ChiXin Ger 1 69.6 US 1 Bel 2 Bel 1 US 2 Hol 3 100.0 Jap 1 Hol 2 Jap 2 Hol 1 Pol 2 Can Tur 1 RusAst 100.0 Tur 2 Tur 3 A2 RusTVe 1 100.0 ChiXu 1 RusTom ChiFe 3 53.0 ChiFe 2 87.4 RusRya 2 ChiFe 1 RusRya 1 ChiXu 2 RusNov 1 69.2 63.0 ChiLiu 1 RusMosc ChiLiu 2 B1 ChiLiu 3 ChiXu 2 100.0 ChiQ 1 ChiXu 1 ChiQ 3 87.7 ChiQ 2 ChiQ 2 ChiXin ChiQ 1 93.2 Jap 1 100.0 100.0 Jap 3 ChiLiu 2 Jap 2 B2 ChiLiu 1 US 1 ChiFe 2 100.0 US NCBI US 2 C ChiFe 1 NCBI AY075048 Polyphermus pediculus Podon leuckarti NCBI DQ889121 Evadne nordmanni 10 10

Figure 2 Phylogenetic estimate of Leptodora using maximum parsimony. Numbers on the nodes are bootstrap values for (a) the cyto- chrome c oxidase subunit I (COI) gene and (b) the elongation factor-1a (EF1a) gene. The clades identified are the same as for the Bayesian estimate.

364 Journal of Biogeography 38, 359–370 ª 2010 Blackwell Publishing Ltd Biogeography and evolution of Leptodora

The best-fitting model selected by MrModeltest 2.3 for mum 30.65%; Costa et al., 2007). The lowest distance, between the EF1a data set was SYM+G with a relative AIC weight of A1 (Euro-Siberian clade) and A2 (Anatolian clade) reaches 0.6213, and gamma distribution shape parameter 0.4749. The 4.48%, significantly higher than average intra-specific variation sequence data were analysed in the same manner as the COI in crustaceans (0.46%) (Costa et al., 2007). data, with Podon leuckarti (AF526287) and Evadne nordmanni The COI and EF1a sequences from 28 Palaearctic popula- (AF526288) as outgroups. All phylogenetic analyses of the tions yielded 38 haplotypes (Figs 3 & 4), the majority of which EF1a data set revealed two major clades: one corresponding to are in the COI gene. Some of these were present in different clade A of the COI trees, while the B and C mitochondrial populations (H17, H11 and H31). Thirteen out of 28 clades appeared together as one EF1a clade. Further inspection populations had two or more haplotypes, reflecting a genetic of the two trees shows that the main difference between both is subdivision within populations. The Xinjiang population, for a somewhat more conserved status of the EF1a gene. example, had four private COI haplotypes among five Moreover, all populations from the Siberian and eastern specimens analysed (H25–H28). Only the populations from European plains (except the Baltic population of Pskov, and Austria and Hungary, separated by a narrow geographic gap, the ‘Central Asian’ population of Wulungu Lake, Xinjiang) are shared a single identical COI haplotype (H11). shifted from clade A to clade B. Molecular clock COI divergence and haplotypes The trees obtained by running dnaml and dnamlk were The uncorrected K2P pairwise distances among COI clades similar, with log likelihoods of )2309.6 (dnaml) and )2335.4 varied between 4.48% and 17.30%. The highest distance, (dnamlk). Thus, the log likelihood was not significantly between C (North American clade) and A2 (Anatolian clade), increased under the constraint of a molecular clock (chi-square reached 17.30%, and is similar to the mean congeneric distance test: for n = 68, n ) 2 = 66, v2 = 51.6, and P > 0.9, such that in Crustacea (17.16%; in , minimum 13.18%, maxi- the hypothesis of a clock being operative is accepted).

A1 RusMosc H23545 RusPsk H21 585 585 586 545 584 RusTve H22 RusNov H19 RusTve H18 Rom H6 587 173 A2 331 640 80 81 Pol H7 Bel H5 RusRya H16 RusTom H17 RusTve H18 529 477 77 119 28 Tur H28 469 557 ChiWu H26 482 166 469 178 637 88 382 293 ChiWu H24 ChiWu H27 Pol H3 307 Ger H1 481 211 304 304 178 514 373 Ger H2 Hol H4 ChiWu H25 637 514 340 340 40 17 85 Hun H11 184 184 IreD H9409 IreD H8 371 229 85 304 C 325 622 82 301 4 49 Fra H12 Slo H15 87 US H29 48 632 632 IreD H10 Fra H13 Slo H14 4 622 85 301 304 93 622 624 628 223 484 532 631 103 ChiFe H34 ChiXu H30 ChiXu H32 Jap H35469 Jap H36 623 627 622

484 490 490 223 46 490 106 ChiQ H31 352 Jap H37 454 B1ChiLiu H33 B2

Figure 3 Haplotype network for Leptodora based on the cytochrome c oxidase subunit I (COI) gene. The subnetworks identified corre- spond to the clades of Fig. 1 and include the USA, Turkey, Japan, China and a Euro-Siberian network that includes a population from Xinjiang, China. Numbers between nodes indicate the position of mutations in the alignment. Numbers between subnetworks represent the average number of mutations between subclades.

Journal of Biogeography 38, 359–370 365 ª 2010 Blackwell Publishing Ltd L. Xu et al.

Aus h3

9 670

Aus h2 Ger h1 388 4 ChiWu h5 670 9

685 2 18 27 36 37 43 12 Slo h11 Slo h10 Hol h4 RusPsk h18 417 5 10 Fra h8 Bel h6 438 438 10

Fra h9

12

US h22348 US h21 768

24 24

RusAst h23 474 474 Can h16 208 24

768 804 438 587 3 RusMosc h20 RusRya h18 714 Jap h17 309 354 373 415 549 729 348 804804 2 543 RusTom h19 612 3 516 ChiXin h13 ChiXu 10 h12 256

RusKha h14 7

RusKha h15

Figure 4 Haplotype network for Leptodora based on the elongation factor-1a (EF1a) gene. Two subnetworks were identified: a European one, which includes a population (RusPsk) from the Baltic area of Russia but none of the other Russian populations, and the population from Xinjiang, China (ChiWu). All other Russian and Siberian populations appear in the second network, which is composed of populations from China, Japan, Siberia and North America.

At that time, the cooling of a generally warm climate that had DISCUSSION started in the Oligocene was accelerated by the uprising of the , Altai and similarly aged mountain chains; the part Phylogeographic patterns and speciation in Leptodora of the Leptodora range situated in eastern China is currently Since Leptodora extends from western Europe to eastern closest to that ancestral situation. Ancestral Leptodora-like Siberia, East Asia including Japan, and North America it had to haplopods evolved in a climate warmer than today, and for extend across Beringia until climatic cooling eliminated it from that reason the relatively thermophilic East Asian L. richardi there. Currently, it may occur further north in Siberia than in may be closest to the stem form. Japanese (B2 clade) and Alaska, reflecting the thermal properties of the Siberian hybrid Turkish (A2 clade) populations that accumulated fewer cited earlier. mutations seem to have become isolated since the early Looking at the number of mutations between the three main Pleistocene. In the case of the Japanese population, persistent clades (Fig. 3), and applying the conventional mitochondrial insularity (and the incapacity of Leptodora to cross marine ) COI molecular clocks for Crustacea (1.4–2.3% Myr 1 in barriers, as exemplified by its absence from Iceland) seems to ) calanoid , Dooh et al., 2006; 1.4–2.6% Myr 1 in have contributed to isolation. The Irish population, in Gammarus, Hou et al., 2007), the divergence between the contrast, appears to have been isolated since the most recent Euro-Siberian and East Asian lineages dates back to 6.3– deglaciation only, and is genetically indistinguishable from 12.2 Ma, and that between the East Asian and North American populations on the European mainland. lineages to 3.9–8.2 Ma. The most recent common ancestor of Korovchinsky’s (2009) L. richardi from the Heilong–Amur, these lineages should therefore date back to the (late) Miocene. eastern China and Japan is morphologically hard to separate

366 Journal of Biogeography 38, 359–370 ª 2010 Blackwell Publishing Ltd Biogeography and evolution of Leptodora

(mainly using chaetotaxy, and conditional to examining a fair and Stanovoy ranges in the north-east, created a wall of series of individuals) from L. kindtii, yet is supported by our mountains that Leptodora could not cross, and behind which molecular information. The region of the COI gene sequenced Central Asian high plateaus and aridity raised a second barrier. by us is also used in DNA barcoding (Hebert et al., 2003, 2004; Only near the far-eastern Heilong Valley are the mountains Costa et al., 2007), using K2P sequence divergences to decide low enough to be crossed. However, the wall is also breached at on speciation. In crustaceans, inter-generic divergences are another point, of considerable historical and biogeographic often in excess of 8%. Our study showed K2P gaps between the interest, known as the Dzungarian Gates (De Lattin, 1967; A, B and C clades of Leptodora of up to 17.30% (maximum Dumont, 2003) (Fig. 5). Here, the Irtysh River, draining the divergence was between North American and Anatolian Mongolian south Altai to the arid Dzungarian Basin, flows clades). A lower divergence (4.48%) was found between the through an opening between the Altai, Dzungar and Tien Shan A1 (Euro-Siberian clade) and A2 (Anatolian clade), suggesting mountains, to join the River in Siberia. All other rivers an infra-specific rank for the eastern Mediterranean popula- inside the Dzungarian Basin are currently endorheic. These tion. The same is true of the insular Japanese populations include the Wulungu River, a former tributary of the Irtysh, of (Table 2). So, based on COI, we conclude that the main which Lake Wulungu (or Ulungu) is currently the endpoint. lineages in our study represent three species and two probable Because it is closed, this lake is slightly saline (current salinity ) subspecies. Of the three species-level taxa, only the North c.2g L 1), and has been in this condition throughout the American is provisionally without a name. However, by Holocene (Liu et al., 2008). Climate changes did occur (Jiang analogy with discoveries in North American Holopedium et al., 2007), but were not incisive enough to reconnect the (Rowe et al., 2007) and Polyphemus (Xu et al., 2009), it is lake to the Irtysh. likely that future work will disclose deep divisions and several Geologically, the Wulungu Valley formed after the Altay cryptic taxa there as well. uplift, and took its present shape in mid-Quaternary times Leptodora avoids arctic temperatures, but its dispersal is also (Mao, 1981). As long as the Wulungu River was still connected obstructed by mountain chains. The mid to late Cenozoic to the Irtysh there was a possibility for Leptodora to colonize a Alpine folding, from the Alps in the south-west to the Altai precursor of Lake Wulungu. However, once the link between

Table 2 Genetic diversity, assessed by Kimura’s two-parameter distance (median, in %) within/between the five cytochrome c oxidase subunit I (COI) clades of Leptodora with uniform rates; standard error estimates obtained by a neighbour-joining bootstrap procedure with 10,000 replicates.

A1 A2 B1 B2 C Outgroup

A1 1.00 ± 0.2 A2 4.48 ± 0.79 0.00 B1 16.53 ± 1.76 16.31 ± 1.82 0.36 ± 0.13 B2 17.01 ± 1.86 16.66 ± 1.86 8.28 ± 1.20 0.54 ± 0.24 C 15.22 ± 1.70 17.30 ± 1.87 10.18 ± 1.35 11.48 ± 1.44 0.11 ± 0.11 Outgroup 28.15 ± 2.28 28.63 ± 2.31 27.84 ± 2.30 27.40 ± 2.24 27.85 ± 2.26 18.58 ± 1.93

Figure 5 phylogeographic structure of Leptodora. Leptodora richardi occurs in East Asia including Japan (grey dots). Leptodora kindtii is found in central and western Europe (black dots). The wide zone between both (black and grey dots) is inhabited by hybrids (females of L. kindtii · males of L. richardi). The only exception is the population of Lake Wulungu. This is pure L. kindtii, which crossed the Dzungarian Gates (DZ G, arrow) during a humid climatic spell. When the climate became drier, it became isolated in the endorheic basin of the Wulungu River.

Journal of Biogeography 38, 359–370 367 ª 2010 Blackwell Publishing Ltd L. Xu et al. lake and river was severed it never became re-established (Mao, The reduced genetic variation found from Moscow to the 1981), assigning a maximum age of isolation to the local Heilong Valley (not much more than in the single population Leptodora population. The four private haplotypes that we of Lake Wulungu) further suggests that hybridization occurred found are an expression of this isolation (Fig. 3). The during a brief, comparatively recent period, with the mothers mitochondrial COI molecular clock used earlier places its of the hybrids clearly derived from western European stock divergence at 0.4–0.7 Ma, and this agrees well with Mao’s (Fig. 5). Thus, we have a case in which Europe (but not the (1981) geological information. The early origin of the Lake Mediterranean zone) acted as a refugium and only part of its Wulungu population is reinforced by another argument: a diversity (alleles) expanded to the recolonized area (Siberia), a comparison of the two genes studied shows that it is pure familiar phenomenon in post-glacial reinvasions (Sommer & L. kindtii, not a hybrid between L. kindtii and L. richardi (see Zachos, 2009). The western European populations, more cold- below). adapted than the eastern ones, reacted first to deglaciation and Palaeolimnological information offers yet another possibility invaded new territory. Their latest expansion may therefore be for dating the Wulungu population, by identifying a period as recent as 12 ka (Hewitt, 2000). wet enough to open most of the currently endorheic lakes of On the other hand, across the repeated glacial cycles of the Central Asia, and the Caspian Basin is the candidate of choice Pleistocene, there may have been several advances and retreats for this. The lake level, currently at )26 m, fluctuated strongly of Leptodora. During one of these, probably towards the end of across the Pleistocene, but perhaps the longest spell during the Apsheron phase, it managed to cross the Dzungarian Gates, which the Caspian Lake was connected with the Black and and survived in isolation up to the present, accumulating Lake Aral and stood at c. +50 m, was the Apsheron period. mutations over time. The hybrids, having the thermal prop- This ended around 0.7 Ma (Dumont, 1998; Boomer et al., erties of L. kindtii, were quite successful at expanding 2000). westwards, suppressing the mother species, and currently There is no indication that Leptodora expanded into China cover more than two-thirds of the full range. Under unchanged from the Wulungu Basin. Apparently, it was stopped by climate conditions, they may soon cover the entire range of persistent local and semi-deserts, such that contacts L. kindtii. However, they failed to cross the Dzungarian Gates, between L. kindtii and L. richardi could only take place via the or at least could not reach the now disconnected Lake Heilong Basin in the east (Fig. 5). However, it cannot be Wulungu, leaving behind an isolated colony of L. kindtii that excluded that isolates similar to the one of Lake Wulungu exist could embark on an evolutionary pathway of its own. elsewhere in Siberia. Lake Balkash in Kazakhstan is also a candidate, as are the lakes of the southern Caucasus, and the CONCLUSIONS Kashmir populations mentioned earlier. The history of the extant Leptodora unfolds as a complex story that may begin with the alpine folding in the late Hybridization Miocene, when an ancestral form extended from western An intriguing finding of this study is the discovery of a Europe over most of northern and Central Asia, Beringia and hybrid zone between L. kindtii and L. richardi, extending North America. –Pleistocene cooling first severed the from west of Moscow and Astrakhan (the Volga valley) North American–Eurasian contact. Unlike other cladocerans, across almost the full width of Siberia (Fig. 5). Morpholo- e.g. Eubosmina (see Haney & Taylor, 2003), the Nearctic form gically, the hybrids are hard to identify, a phenomenon also is therefore not a recent invasion from the Palaearctic. noted in Daphnia (Dlouha et al., 2010). They have mito- Additionally, it isolated a thermophilic clade (richardi)in chondrial DNA typical of L. kindtii, with no immixture of eastern Asia from an Euro-Siberian clade, of which the L. richardi. However, the nuclear EF1a from west of western subclade is particularly well cold-adapted. The Moscow to Khabarovsk is of L. richardi, while further vagaries of the Pleistocene climate produced new disjunctions south, in China and Japan, there is no trace of a mixing of within the two Eurasian clades, with at least two isolates the L. richardi nuclear genome with that of L. kindtii. (Japan and the eastern Mediterranean). During glaciations, Because mitochondrial DNA is maternally inherited, this the ranges contracted, whereas during deglaciations they zone is due to sexual L. kindtii females mating with expanded and met. During one of the eastward expansions of L. richardi males, and not vice versa. Leptodora reproduces L. kindtii it crossed the Dzungarian Gates, and became parthenogenetically during summer and sexual stages appear isolated in a currently in Xinjiang. The ranges only briefly at the end of the season, requiring higher of L. kindtii and L. richardi last met in the Heilong Valley, temperatures in L. richardi than in L. kindtii.IfL. kindtii possibly during the last hypsithermal, and a wave of hybrids males are not produced at exactly the same time as the involving descendants of a cross between L. richardi males L. richardi sexual females, neither ever meet and hybridiza- and L. kindtii females subsequently rolled westwards over tion will not occur. Conditions for a successful hybridization Siberia. Hybrids currently cover more than two-thirds of the were probably satisfied during the Holocene hypsithermal, Eurasian Leptodora range, and might suppress western and it may thus have occurred from 10 ka onwards and European populations, leaving only some isolates (such as stopped when the climate cooled thereafter. in Lake Wulungu) of pure L. kindtii.

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