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Genetic and Morphological Differentiation of Dikerogammarus Invaders and Their Invasion History in Central Europe

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Genetic and Morphological Differentiation of Dikerogammarus Invaders and Their Invasion History in Central Europe Freshwater Biology (2002) 47, 2039–2048 Genetic and morphological differentiation of Dikerogammarus invaders and their invasion history in Central Europe JAKOB C. MU¨ LLER, STEPHANIE SCHRAMM and ALFRED SEITZ Institute of Zoology, University of Mainz, Mainz, Germany SUMMARY 1. Biological invasions often involve close taxonomic relatives either as native ⁄ invader pairs or as invader ⁄ invader pairs. Precise identification and differentiation of species is therefore of paramount importance to reconstruct the invasion history. Genetic studies are indispensable in the case of morphologically conservative taxonomic groups. 2. We analysed the Pontocaspian freshwater amphipods Dikerogammarus that have successfully invaded the benthos of large Central European rivers. Taxonomic uncertainties were clarified by phylogenetic analyses of mitochondrial 16S and COI genes. The three-way partitioning of allozyme genotypes in a syntopic population further corroborated the taxonomic status of the three species Dikerogammarus haemobaphes, D. villosus and D. bispinosus. Dikerogammarus bispinosus had been prior misidentified as a subspecies of D. villosus. The conspicuous colour types of D. villosus, however, appeared to be conspecific. 3. The genetic identification of the previously more abundant D. haemobaphes individuals in old samples supported the ‘successive invasion wave’ hypothesis with D. haemobaphes as the first invader displaced by the second invader D. villosus. Dikerogammarus bispinosus could be a potential future invader. 4. Haplotype differentiation was apparent between two invasion lines of D. haemobaphes, but the occurrence of a single widespread haplotype indicates genetic impoverishment during rapid colonisation. Keywords: biological invasions, colour types, Crustacea, freshwater amphipods, mtDNA are in doubt (Marsden, Spidle & May, 1996). Only Introduction genetic studies could clarify the taxonomic problems Taxonomic misdetermination may obscure the true and stimulate further investigation to discover diag- history of invasion patterns when close relatives are nostic morphological traits. involved. The Dreissena invasion of North America is Concurrent immigration of closely related taxa is a good example. Between the first appearance of common in European waters (Kinzelbach, 1995). dreissenid mussels in 1988 and the genetic identifica- Examples are the species groups of Corbicula, Viviparus, tion of a second species Dreissena bugensis in 1992 Jaera and Dikerogammarus in the highly invaded Central (May & Marsden, 1992) all individuals were assumed European large rivers (Tittizer, 1996). Taxonomic to be Dreissena polymorpha. For this period, life history uncertainties are particularly conspicuous among taxo- experiments, specific invasion protocols and even nomic groups originating from remote areas when genetic inferences about founder and heterosis effects taxonomic literature is not readily available. In Central Europe, most of the riverine invaders come from the Correspondence: Jakob C. Mu¨ ller, Institute of Human Genetics, species-rich Pontocaspian region via either the Dnjepr GSF-National Research Center for Environment and Health, or Danube rivers. In particular, the systematics of 85764 Neuherberg, Germany. E-mail: [email protected] freshwater amphipods is difficult (Barnard & Barnard, Ó 2002 Blackwell Science Ltd 2039 2040 J.C. Mu¨ller et al. 1983), because of their morphological conservatism The present study aims to clarify the diversity of and presumably high speciation rate (Mu¨ ller, 2000). Central European Dikerogammarus invaders by analy- Imprecise taxonomy makes inferences about the ses of genetic markers. In view of the uncertain original distributions of described taxa also doubtful taxonomic status of subspecies and colour morphs, we (Mordukhai-Boltovskoi, 1964; Jazdzewski, 1980). test whether those involved in the Central European Two species of the amphipod genus Dikerogamma- invasion merit species status. Dikerogammarus villosus rus are extraordinarily successful invaders in Europe. bispinosus, which was also recorded from the lower Dikerogammarus haemobaphes (Eichwald, 1841) invaded Danube (Ponyi, 1958) is suspected to be a potential the upper Danube around the middle of the 20th candidate. Because of the short documentation period century (Nesemann, Po¨ckl & Wittmann, 1995) and of D. haemobaphes in the Rhine area, a misdetermin- was the first discovered in the Rhine drainage ation could not be excluded. The present genetic immediately following the 1992 opening of the analysis of historical samples may therefore corrobor- Main-Danube-canal (Schleuter et al., 1994; Tittizer, ate the hypothesis of successive invasion waves of the 1996). Dikerogammarus haemobaphes also immigrated two Dikerogammarus species. In addition, the geo- to Central Europe from the Dnjepr river (Jazdzewski graphical distribution of genotypes will allow some & Konopacka, 2000). Dikerogammarus villosus (Sowinsky, inferences to be made about the invasion process. 1894) was recorded in the upper Danube in the late 20th century and was found in the Rhine system about 1 year after D. haemobaphes (Nesemann et al., 1995; Bij Methods de Vaate & Klink, 1995; Scho¨ll, Becker & Tittizer, Sampling and morphological typing 1995). The larger D. villosus has now displaced D. haemobaphes at most locations in the upper Danube Dikerogammarus specimens were collected widely in and Rhine system and has successfully colonised the Central Europe, including the lower Danube (Fig. 1). large rivers in northern Germany and France (perso- The southern invasion route (Danube) was intensively nal observations; Grabow, Eggers & Martens, 1998; sampled around the Main-Danube-canal, and the nor- Devin et al., 2001). thern invasion route was considered by sampling a Fig. 1 Sampling locations mapped on the Central European waterways. Ó 2002 Blackwell Science Ltd, Freshwater Biology, 47, 2039–2048 Differentiation of Dikerogammarus invaders 2041 population in the river Vistula. Most sampling was gene we used the primers COIa-H (Simon, Franke & performed in May–August 1997 (RHI, MA1-MA8, Martin, 1991) and COI-Gf (Meyran, Monnerot & KA1-KA2, DA1-DA4, DUN and BUN) and in April– Taberlet, 1997). The PCR products were purified October 1998 (VIS, DEV, NU¨ R, LIN). Additional sam- using a microspin method and sequenced using the ples were collected in March ⁄ April ⁄ August 2000 (SAO, dye terminator cycle method (ABI PRISM BigDye kits) BRA, BSC) and spring 1996 (M96 near location MA2). with following gel electrophoresis on an automated Adult individuals were randomly collected from all sequencer (ABI PRISM 377). The haplotype sequences potential microhabitats near the riverbanks of each were submitted to the EMBL ⁄ GenBank ⁄ DDBJ data- site. Individuals from RHI, MA1-MA8, KA1-KA2, base (Accession Nos. AJ440887–AJ440921). DA1-DA4 and DUN were frozen in liquid nitrogen to be used for both allozyme and mtDNA analysis. The Statistics other specimens were stored in pure ethanol and were typed for mtDNA only. Specimens were identified to Genetic differentiation between the D. villosus colour species using the diagnostic morphological features types was tested with an exact test using GENEPOP according to Carausu, Dobreanu & Manolache (1955) (Raymond & Rousset, 1995) after all populations in and Ponyi (1956) prior to genetic analyses. Frozen the allozyme analysis were pooled and then sorted by D. villosus were classified according to their colour colour types. types (Nesemann et al., 1995). Based on the ideas of Buth (1984), we performed a parsimony cluster analysis on the syntopic population DUN to test the genetic three-way partitioning. Allozyme and mtDNA procedures Different multilocus-genotypes were listed and sin- Homogenates of half individuals were used for allo- gle-locus-genotypes were coded to allow one consis- zyme electrophoresis according to the methods of tent symmetric stepmatrix. The number of steps Hebert & Beaton (1989) and Mu¨ ller (1998). After between character states were given values between screening 30 enzyme systems, the following 9, well- 0 and 2: 0 means no change of single-locus-genotype; interpretable, enzyme loci were selected for the 1 means only one allele is different (e.g. between analysis: ACON (E.C. 4.2.1.3), APK (E.C. 2.7.3.3), genotypes aa and ab) and 2 means both alleles are GOT (E.C. 2.6.1.1) with the faster locus GOT-I and different (e.g. aa and bc). Most-parsimonious trees of the slower locus GOT-II, GPI (E.C. 5.3.1.9), G3PDH all multilocus-genotypes were generated from 500 (E.C. 1.2.1.12), MPI (5.3.1.8), PGM (E.C. 5.4.2.2) with replicates of random addition sequences for heuristic the faster PGM-f and the slower PGM-s. About 50 searches using PAUP (Swofford, 1993). Bootstrap individuals per population were typed for these frequencies were obtained by 1000 replicates of allozymes. heuristic searches with simple addition sequences. Two to 11 individuals of each of the 16 populations Mitochondrial DNA sequences were aligned by the representing the whole sample area were sequenced Clustal W program according to the algorithm des- at two mitochondrial genes. Animals were homo- cribed in Thompson, Higgins & Gibson (1994). The genised with a microspatula and total DNA was most-parsimonious trees were found by exhaustive extracted by a silica gel-based spin column procedure. searches using PAUP. Gaps were treated as fifth base The conditions of the subsequent polymerase chain and all mutations were weighted equally. Bootstrap reaction (PCR) are outlined
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