Round Goby Phylogeography
During the past two decades, the Eurasian round goby Neogobius melanostomus (=Apollonia melanostoma) has expanded its range via shipping transport and canals, extending north and westward from the Ponto-Caspian region and to the North American Great Lakes. The objective of this study was to examine the round goby's genetic variation across its native and nonindigenous Eurasian and North American ranges (Fig. 1 & 2), in order to evaluate its present day and historical biogeography. Data from 8 nuclear microsatellite loci and mitochondrial DNA cytochrome b gene sequences are analyzed from 1200+ individuals in 48 locations to elucidate genetic divergence patterns in relation to geological history and recent expansion pathways. Population structure is evaluated using FST-analogs, phylogenetic trees, clustering diagrams, Bayesian assignment tests, and nested clade analyses. Native populations in the Black versus the Caspian Sea basins are markedly diverged (1.4%, ~0.7 - 1.4 mya, see Figs. 3-5), corresponding to geological separation during early to mid Pleistocene low waters. Primary watersheds within each basin diverge by ~0.4% (~0.2 to 0.4 my), dating to Black Sea marine transgression and formation of the modern Volga River in the Caspian Sea. Most native populations average higher genetic variability (0.58 ± 0.08) than do non-native sites (0.25 ± 0.15); however, exotic locales in the upper Dnieper River and the Moskva River (of the Volga system) have high diversity (0.54 and 0.86). Exotic populations in the Danube and Dnieper Rivers and the Baltic Sea trace to separate northern Black Sea regions, whereas those in the upper Volga River system are a mixture of Black and Caspian Sea lineages (Fig. 4).
North American populations have 1-6 haplotypes compared with 1-11 in native Eurasian locations. Samples from Lake Superior, Georgian Bay, the Erie Canal and the St. Lawrence River had relatively low gene diversity, suggesting their establishment by only a few individuals and severe bottlenecks (Fig. 6). Significant differences among several Great Lakes locations and differential assignments to various putative Eurasian sources within the Black Sea basin (Fig. 6) suggest that multiple founding sources and introductions were involved. The central Great Lakes populations showed significant correspondence to a likely source population near the mouth of the Dnieper River. The Bay of Quinte population in Lake Ontario was distinct from other North American populations (Fig. 6). Appreciable genetic diversity likely contributed to the invasive success of the round goby. Some genotypes in the Great Lakes also are common in Black Sea marine populations, suggesting that the round goby may become established in estuarine habitats along North American coasts, given the opportunity.
Figure 1. Eurasian round goby distribution (hatched areas), showing sampling locations (lettered). Filled symbols denote introduced locations, open symbols represent native locations. Locations in the Black and Caspian Sea clades are represented by circles and squares, respectively.
Figure 2. North American round goby distribution (hatched areas), showing sampling locations. All North American samples nest within the Black Sea clade in nested clade analysis.
Figure 3. Neighbor-joining tree of phylogenetic relationships among common Eurasian round goby Neogobius melanostomus haplotypes (found in multiple individuals), constructed in MEGA v3.1 (Kumar et al. 2004), and rooted to its monkey goby sister species (N. fluviatilis) and three other "neogobiin" species. Bootstrap % ≥ 50% pseudo-replications. Branch lengths are proportional to genetic divergence in substitutions/site.
Figure 4. Parsimony network among round goby Neogobius melanostomus haplotypes showing nested clades (NCA: Templeton et al. 1995), depicting division between the Black/Azov and Caspian Seas (clades 5-1 & 5-2) and between Black/Azov lineages (4-1 & 4-2). The monkey goby N. fluviatilis sister species roots to haplotype 37 (*).
Figure 5. Bayesian STRUCTURE v2.1 (Pritchard et al. 2000, Pritchard & Wen 2004) analysis of round goby populations using combined data from seven microsatellite loci and cyt b sequences. K=15 (pp = 0.999). Each individual is represented by a thin vertical line, which is partitioned into K colored segments that represent the individual’s estimated membership fractions. Black lines separate individuals from different sampling sites, which are labeled above the figure. Ten STRUCTURE runs at each K produced nearly identical individual membership coefficients, having pairwise similarity coefficients above 0.95, and the figure illustrating a given K is based on the highest probability run at that K. Results show five main population genetic divisions in the Black/Azov Sea basin and three within the Caspian Sea basin.
Figure 6. Bayesian STRUCTURE v2.1 (Pritchard et al. 2000, Pritchard & Wen 2004) assignment test of the relationships among North American and Eurasian locations using 7 microsatellite loci and cyt b data (N = 680). This analysis reveals finer scale relationships than the statistical parsimony network, showing considerable genetic structure in North America.
Brown, J.E. and C. A. Stepien. 2008. Ancient divisions, recent expansions: Phylogeography and population genetics of the round goby Apollonia melanostoma across Eurasia. Molecular Ecology 17:2598-2615.
Brown, J.E. and C.A. Stepien. 2009. Invasion genetics of the round goby: Tracing Eurasian source populations to the New World. Molecular Ecology 18:64-79.