Changes in Genetic Structure of North American Bythotrephes Populations Following Invasion from Lake Ladoga, Russia
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Freshwater Biology (2002) 47, 275–282 Changes in genetic structure of North American Bythotrephes populations following invasion from Lake Ladoga, Russia DAVID J. BERG,* DAVID W. GARTON,† HUGH J. MACISAAC,‡ VADIM E. PANOV§ and IRENA V. TELESH§ *Department of Zoology, Miami University, Hamilton, OH, U.S.A. †School of Biology, Georgia Institute of Technology, Atlanta, GA, U.S.A. ‡Department of Biological Sciences and Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ont., Canada §Zoological Institute of the Russian Academy of Sciences, St Petersburg, Russia SUMMARY 1. We used allozyme electrophoresis to compare Bythotrephes longimanus (Crustacea: Onychopoda: Cercopagididae) from recently founded North American populations with those from native European populations, and to examine changes in genetic structure of North American populations over time. 2. The genetic structure of North American populations in 1996 was similar to that of European populations, because of the disappearance of founder effects which distin- guished North American from European populations in 1989. 3. The Lake Ladoga, Russia population was more closely related to North American populations than to other European populations, consistent with non-genetic evidence implicating Lake Ladoga as the source of North American populations. 4. Our results provide additional evidence of the presence of an invasion corridor that allows Urasian and Ponto-Caspian species to be introduced into North American freshwater ecosystems, and show that founder effects can erode over time following establishment of invasive species. Keywords: exotic species, founder effect, genetic structure, Great Lakes invasion corridor notorious invader is the sea lamprey [Petromyzon Introduction marinus (L)], which devastated native fish populations The introduction of exotic species into novel environ- in the mid-20th century (Smith & Tibbles, 1980). Most ments is a major concern of scientists studying the recently, these ecosystems have experienced a spate of effects of human activities on ecosystems (Vitousek Eurasian species becoming established during the et al., 1997; Cohen & Carlton, 1998). The Laurentian 1980s and 1990s. Prominent examples of recent intro- Great Lakes have become home to a number of exotic ductions are fishes such as ruffe [Gymnocephalus organisms following the arrival of Europeans, with cernuus (L)] and round goby (Neogobius melanostomus many of these species causing marked changes in Pallas), zebra and quagga mussels (Dreissena polymor- the lakes’ ecosystems (Mills et al., 1993). The most pha Pallas and D. bugensis Andrusov, respectively), and other benthic and planktonic invertebrates Correspondence: David J. Berg, Department of Zoology, Miami (reviewed in Mills et al., 1993; MacIsaac, 1999). The University, 1601 Peck Blvd, Hamilton, OH 45011, U.S.A. mode of introduction of these exotic species is believed E-mail: [email protected] to be discharge of freshwater ballast transported Ó 2002 Blackwell Science Ltd 275 276 D.J. Berg et al. from European waterways via ocean-going freighters comutase (PGM) locus and low levels of variation (Sprules, Riessen & Jin, 1990; Mills et al., 1993). among populations (Weider, 1991; Berg & Garton, Bythotrephes sp., a Palearctic zooplankter, was first 1994). found in the Great Lakes in 1982 (Johannsson, Mills & Population genetic theory predicts that newly O’Gorman, 1991). Initially identified as B. cederstroemi established populations will exhibit founder effects, Schoedler, recent work has shown that this taxon is including loss of genetic variation and/or alteration of conspecific to B. longimanus Leydig (see discussion in genetic structure from passing through a bottleneck, if Yan & Pawson, 1998 and MacIsaac et al. 2000). Lake the founding population is small. Founder effects Ladoga, Russia was implicated as a probable source have been noted in a number of aquatic invertebrate of this exotic species because of its direct connection taxa that show high levels of allele frequency diver- to the harbour of St Petersburg and the eastern Gulf gence among populations (Boileau, Hebert & of Finland via the Neva River, and because freighters Schwartz, 1992; DeMelo & Hebert, 1994). Low levels bound for Great Lakes ports often take on ballast of interpopulation genetic variation and heterozygote water at St Petersburg (Sprules et al., 1990). At many excesses found in North American populations of times of the year, this ballast is fresh or oligohaline B. longimanus probably represent a founder effect due water because of the low salinity of the eastern Gulf to the numerical dominance of some clonal groups of Finland, which is strongly influenced by the Neva (multiple locus genotypes) with a heterozygous geno- River, a major tributary of the Baltic Sea. The type at the PGM locus. zooplankton community in Neva Bay, a part of St We used allozyme electrophoresis to survey genetic Petersburg Harbour, is composed primarily of popu- variation in B. longimanus populations from the lations that originate in Lake Ladoga and are Laurentian Great Lakes and Lake Ladoga. Samples transported to the bay via the Neva River (Telesh, were collected in 1996, 9–12 years after invasion of the 1995). Thus, the potential exists for ship-mediated Great Lakes. We compared these results with an transcontinental transport of freshwater and euryha- earlier (1989) allozyme survey of populations from the line organisms between the Lake Ladoga-Neva estu- Great Lakes and other European lakes (Berg & Garton, ary-Gulf of Finland system and the Laurentian Great 1994) to determine whether Lake Ladoga was the Lakes. probable source of the North American populations, Like most cladocerans, B. longimanus is a cyclic and to assess the stability of the unique genetic parthenogen. The primary mode of reproduction is structure of the Great Lakes populations. clonal, interspersed with bouts of sexual reproduction under stressful environmental conditions, especially Methods during late autumn (Hebert, 1987). As such, new populations can be established by the introduction of Bythotrephes longimanus were collected from Lakes as few as one female individual. Large-lake popula- Ladoga, Superior, Michigan, and the North Channel tions of cladocerans are characterised by stable allele and main basin of Lake Huron from 28 July to 23 frequencies with genotypic arrays meeting Hardy– August 1996, using a 500-lm mesh plankton net. Weinberg expectation (HWE) because of regular Captured individuals were preserved in a 15% episodes of sexual reproduction (reviewed in De trehalose solution (Taylor, Finston & Hebert, 1994). Meester, 1996). A previous study of Bythotrephes Standard cellulose acetate electrophoresis techniques found that populations from European lakes con- (Hebert & Beaton, 1989) were used to measure tained relatively low levels of intrapopulation genetic genetic variation at nuclear loci. Loci surveyed were variation compared with other cladocerans, but that alkaline phosphatase (ALP, EC 3.1.3.1), fumarase genotype frequencies met HWE (Berg & Garton, (FUM, 4.2.1.2), glutamate oxaloacetate transferase 1994). Interpopulation variation was low within (GOT, 2.6.1.1), isocitrate dehydrogenase (IDH, drainage basins but high among basins in Finland 1.1.1.42), leucyl-alanine peptidase (PEP, 3.4.11), and Germany. In contrast, 2–5 years old North malate dehydrogenase (MDH, 1.1.1.37), malic enzyme American populations were characterised by geno- (ME, 1.1.1.40), mannose phosphate isomerase (MPI, type frequencies that were different from HWE as a 5.3.1.8), (PGM 5.4.2.2), and phosphoglucose isomerase result of heterozygote excesses at the phosphoglu- (PGI, 5.3.1.9) for all populations. Sample sizes Ó 2002 Blackwell Science Ltd, Freshwater Biology, 47, 275–282 Bythotrephes genetic structure 277 were 34–79 individuals per population. Data were expected frequencies were then compared with the analysed using Biosys-1 (Swofford & Selander, 1981) frequencies found in the 1996 North American and Tools for Population Genetic Analysis (Miller, populations using R · C contingency tables. 1998). Polymorphic loci were defined as those in which the most common allele was present at a Results frequency £ 0.95. Results were compared with those from a previous Seven of the 10 loci sampled in 1996 had variation study of Bythotrephes (Berg & Garton, 1994), in which present. Two loci (PEP and PGM) were polymorphic, sample sizes varied between 17 and 91 individuals per while rare alleles were found in single North Ameri- population for populations from the same Great Lakes can populations at five loci (FUM, IDH, MDH, ME, sites sampled in this study plus additional sites in PGI; all at frequencies < 0.04). Clonal groups were Lake Erie, south-eastern Finland (four lakes), Sweden identified based on genotypes at the PEP and PGM (one lake), and Germany (two lakes). Two lakes in loci. The PGI locus was polymorphic in several 1989 Finland contained sympatric longimanus-type and European populations, while both the ALP and ME cederstroemi-type individuals; these were treated as loci were polymorphic in one population. separate populations consistent with our earlier study The Lake Ladoga population was more similar to (Berg & Garton, 1994). Great Lakes populations than to European popula- A cluster analysis of the 1996 data with European tions (Fig. 1). Average genetic distance was signifi- populations from 1989 was performed using UPGMA cantly lower between the Great Lakes and Lake to create a dendrogram