, Volume 663, Issue 1, pp 71–82 | Cite as

Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species

  • Elizabeth A. LaRueEmail author
  • Carl R. RuetzIII
  • Michael B. Stacey
  • Ryan A. Thum
Primary research paper


Understanding subsequent dispersal of non-native species following introduction is important for predicting the extent and speed of range expansion and is critical for effective management and risk assessment. Post-introduction dispersal may occur naturally or via human transport, but assessing the relative contribution of each is difficult for many organisms. Here, we use data from seven microsatellite markers to study patterns of dispersal and gene flow among 12 pierhead populations of the round goby (Neogobius melanostomus) in Lake Michigan. We find significant population structure among sampling sites within this single Great Lake: (1) numerous populations exhibited significant pairwise F ST and (2) a Bayesian assignment analysis revealed three distinct genetic clusters, corresponding to different pierhead locations, and genetic admixture between these clusters in the remaining populations. Genetic differentiation (F ST) is generally related to geographic distance (i.e., isolation by distance), but is periodically interrupted at the scale of Lake Michigan due to gene flow among geographically distant sites. Moreover, average genetic differentiation among populations exhibit a significant, negative correlation with the amount of shipping cargo at ports. Our results, therefore, provide evidence that genetic structure of the round goby in Lake Michigan results from limited natural dispersal with frequent long-distance dispersal through anthropogenic activities such as commercial shipping. Our study suggests that while round gobies can undoubtedly disperse and found new populations through natural dispersal mechanisms, their spread within and among the Great Lakes is likely aided by transport via ships. We, therefore, recommend that ballast-water treatment and management may limit the spread of non-native species within the Great Lakes after the initial introduction in addition to preventing the introduction of non-native species to the Great Lakes.


Great Lakes Neogobius melanostomus Ballast water Fish movement Aquatic invasive species Gene flow 



We thank Dustin Wcisel for help in the laboratory and with sampling and Tyler Armstrong for help with the 2008 pilot study. Jeff LaRue, Jordan Allison, Amanda Potter, and Sarah LaRue provided sampling assistance. Yakuta Bhagat, Mark Luttenton, and two anonymous reviewers provided helpful comments on this manuscript. Funding for this project was provided by Grand Valley State University’s Student Summer Scholars program and the Bill and Diana Wipperfurth Student Research Scholarship.

Supplementary material

10750_2010_555_MOESM1_ESM.pdf (67 kb)
Supplementary material 1 (PDF 67 kb)


  1. Bailey, S. A., K. Nandakumar & H. J. MacIsaac, 2006. Does saltwater flushing reduce viability of diapausing eggs in ship ballast sediment? Diversity and Distributions 12: 328–335.CrossRefGoogle Scholar
  2. Bergstrom, M. A., L. M. Evrard & A. F. Mensinger, 2008. Distribution, abundance, range of the round goby, Apollina melanostoma, in the Duluth-Superior Harbor, St. Louis River Estuary, 1998–2004. Journal of Great Lakes Research 34: 535–543.CrossRefGoogle Scholar
  3. Bjorklund, M. & G. Almqvist, 2010. Rapid spatial genetic differentiation in an invasive species, the round goby Neogobius melanostomus in the Baltic Sea. Biological Invasions 12: 2609–2618.CrossRefGoogle Scholar
  4. Brown, J. E. & C. A. Stepien, 2008. Ancient divisions, recent expansions: phylogeography and population genetics of the round goby Apollonia melanostoma. Molecular Ecology 17: 2598–2615.CrossRefPubMedGoogle Scholar
  5. Brown, J. A. & C. A. Stepien, 2009. Invasion genetics of the Eurasian round goby in North American: tracing sources and spread patterns. Molecular Ecology 18: 64–79.PubMedGoogle Scholar
  6. Charlebois, P. M., J. E. Marsden, R. G. Goettel, R. K. Wolfe, D. J. Jude & S. Rudnika, 1997. The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. Illinois-Indiana Sea Grant Program and Illinois Natural History Survey. Illinois Natural History Survey Special Publication No. 20.Google Scholar
  7. Clapp, D. F., P. J. Schneeberger, D. J. Jude, G. Madison & C. Pistis, 2001. Monitoring round goby (Neogobius melanostomus) population expansion in eastern and northern Lake Michigan. Journal of Great Lakes Research 27: 335–341.CrossRefGoogle Scholar
  8. Cookingham, M. N. & C. R. Ruetz III, 2008. Evaluating passive integrated transponder tags for tracking movements of round gobies. Ecology of Freshwater Fish 17: 303–311.CrossRefGoogle Scholar
  9. Cornuet, J. M. & G. Luikart, 1996. Description and power analysis of two tests for detecting population bottlenecks from allele frequency data. Genetics 144: 2001–2014.PubMedGoogle Scholar
  10. Darling, J. A. & N. C. Folino-Rorem, 2009. Genetic analysis across different spatial scales reveals multiple dispersal mechanisms for the invasive hydrozoan Cordylophora in the Great Lakes. Molecular Ecology 18: 4827–4840.CrossRefPubMedGoogle Scholar
  11. Diana, C. M., J. L. Jonas, R. M. Claramunt, J. D. Fitzsimons & J. E. Marsden, 2006. A comparison of methods for sampling round goby in rocky littoral areas. North American Journal of Fisheries Management 26: 514–522.CrossRefGoogle Scholar
  12. Di Rienzo, A., A. C. Peterson, J. C. Garza, A. M. Valdes, M. Slatkin & N. B. Freimer, 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the Academy of Science USA 91: 3166–3170.CrossRefGoogle Scholar
  13. Dufour, B. A., T. M. Hogan & D. D. Heath, 2007. Ten polymorphic microsatellite markers in the invasive round goby (Neogobius melanostomus) and cross-species amplification. Molecular Ecology Notes 7: 1205–1207.CrossRefGoogle Scholar
  14. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefPubMedGoogle Scholar
  15. Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.
  16. Goudet, J. M., M. Raymond, T. Demeeus & F. Rousset, 1996. Testing differentiation in diploid populations. Genetics 144: 1933–1940.PubMedGoogle Scholar
  17. Hayden, T. A. & J. G. Miner, 2009. Rapid dispersal and establishment of a benthic Ponto-Caspian goby in Lake Erie: diel vertical migration of early juvenile round goby. Biological Invasions 11: 1767–1776.CrossRefGoogle Scholar
  18. Hensler, S. R. & D. J. Jude, 2007. Diel vertical migration of round goby larvae in the Great Lakes. Journal of Great Lakes Research 33: 295–302.CrossRefGoogle Scholar
  19. Hubisz, M., D. Falush, M. Stephens & J. Pritchard, 2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9: 1322–1332.CrossRefGoogle Scholar
  20. Hutchinson, D. W. & A. R. Templeton, 1999. Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53: 1898–1914.CrossRefGoogle Scholar
  21. Johnson, L. E. & D. K. Padilla, 1996. Geographic spread of exotic species: ecological lessons and opportunities from the invasion of the zebra mussel Dreissena polymorpha. Biological Conservation 78: 23–33.CrossRefGoogle Scholar
  22. Johnson, T. B., M. Allen, L. D. Corkum & V. A. Lee, 2005. Comparison of methods needed to estimate population size of round gobies (Neogobius melanostomus) in western Lake Erie. Journal of Great Lakes Research 31: 78–86.CrossRefGoogle Scholar
  23. Jude, D. J. & S. F. DeBoe, 1996. Possible impact of gobies and other introduced species on habitat restoration efforts. Canadian Journal of Fisheries and Aquatic Sciences 53(Suppl. 1): 136–141.CrossRefGoogle Scholar
  24. Jude, D. J., R. H. Reider & G. R. Smith, 1992. Establishment of Gobiidae in the Great Lakes basin. Canadian Journal of Fisheries and Aquatic Science 49: 416–421.CrossRefGoogle Scholar
  25. Kipp, R., S. A. Bailey, H. J. MacIsaac & A. Ricciardi, 2010. Transoceanic ships as vectors for nonindigenous freshwater bryozoans. Diversity and Distributions 16: 77–83.CrossRefGoogle Scholar
  26. Locke, A., D. M. Reid, H. C. Vanleeuwen, W. G. Sprules & J. T. Carlton, 1993. Ballast water exchange as a means of controlling dispersal of fresh-water organisms by ships. Canadian Journal of Fisheries and Aquatic Sciences 50: 2086–2093.CrossRefGoogle Scholar
  27. Luikart, G. & J. M. Cornuet, 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12: 228–237.CrossRefGoogle Scholar
  28. Peakall, R. & P. E. Smouse, 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.CrossRefGoogle Scholar
  29. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedGoogle Scholar
  30. Ray, W. J. & L. D. Corkum, 2001. Habitat and site affinity of the round goby. Journal of Great Lakes Research 27: 329–334.CrossRefGoogle Scholar
  31. Raymond, M. & F. Rousset, 1995. GenePop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.Google Scholar
  32. Ricciardi, A., 2006. Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Diversity and Distributions 12: 425–433.CrossRefGoogle Scholar
  33. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.CrossRefGoogle Scholar
  34. Robinet, C., A. Roques, H. Pan, G. Fang, J. Ye, Y. Zhang & J. Sun, 2009. Role of human-mediated dispersal in the spread of the pinewood nematode in China. PLoS One 4: 1–10.CrossRefGoogle Scholar
  35. Sano, L. L., R. A. Moll, A. M. Krueger & P. F. Landrum, 2003. Assessing the potential efficacy of glutaraldehyde for biocide treatment of un-ballasted transoceanic vessels. Journal of Great Lakes Research 29: 545–557.CrossRefGoogle Scholar
  36. Sapota, M. R. & K. E. Skorka, 2005. Spread of alien (nonindigenous) fish species Neogobius melanostomus in the Gulf of Gdansk (south Baltic). Biological Invasions 7: 157–164.CrossRefGoogle Scholar
  37. Schaeffer, J. S., A. Bowen, M. Thomas, J. R. P. French III & G. L. Curtis, 2005. Invasion history, proliferation, and offshore diet of the round goby Neogobius melanostomus in western Lake Huron, USA. Journal of Great Lakes Research 31: 414–425.CrossRefGoogle Scholar
  38. Selkoe, K. A. & R. J. Toonen, 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9: 615–629.CrossRefPubMedGoogle Scholar
  39. Stammler, K. L. & L. D. Corkum, 2005. Assessment of fish size on shelter choice and intraspecific interactions by round gobies Neogobius melanostomus. Environmental Biology of Fishes 73: 117–123.CrossRefGoogle Scholar
  40. Stepien, C. A. & M. A. Tumeo, 2006. Invasion genetics of Ponto-Caspian gobies in the Great Lakes: a ‘cryptic’ species, absence of founder effects, and comparative risk analysis. Biological Invasions 8: 61–78.CrossRefGoogle Scholar
  41. Stepien, C. A., J. E. Brown, M. E. Neilson & M. A. Tumeo, 2005. Genetic diversity of invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Analysis 25: 1043–1060.CrossRefPubMedGoogle Scholar
  42. Suarez, A. V., D. A. Holway & T. J. Case, 2001. Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proceedings of the National Academy of Sciences USA 98: 1095–1100.CrossRefGoogle Scholar
  43. Sylvester, F. & H. J. MacIsaac, 2010. Is vessel hull fouling an invasion threat to the Great Lakes? Diversity and Distributions 16: 132–143.CrossRefGoogle Scholar
  44. U.S. Army Corps of Engineers, 2007. Waterborne Commerce of the United States: Part 3—Waterways and Harbors in the Great Lakes. 1 October, 2009
  45. van Oosterhout, C., W. F. Hutchinson, D. P. M. Willis & P. Shipley, 2004. Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.
  46. Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, E. L. Mills, K. T. Holeck, J. R. Liebig, I. A. Grigorovich & H. Ojaveer, 2002. Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1209–1228.CrossRefGoogle Scholar
  47. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-Statistics for the analysis of population structure. Evolution 38: 1358–1370.CrossRefGoogle Scholar
  48. Whitlock, M. C. & D. E. McCauley, 1999. Indirect measures of gene flow and migration: F ST ≠ 1/(4Nm + 1). Heredity 82: 117–125.CrossRefPubMedGoogle Scholar
  49. Wilson, R. U., E. E. Dormontt, P. J. Prentis, A. J. Low & D. M. Richardson, 2009. Something in the way you move: dispersal pathways affect invasion success. Trends in Ecology and Evolution 24: 136–144.CrossRefPubMedGoogle Scholar
  50. Wolfe, R. K. & J. E. Marsden, 1998. Tagging methods for the round goby (Neogobius melanostomus). Journal of Great Lakes Research 24: 731–735.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Elizabeth A. LaRue
    • 1
    Email author
  • Carl R. RuetzIII
    • 1
  • Michael B. Stacey
    • 1
  • Ryan A. Thum
    • 1
  1. 1.Annis Water Resources InstituteGrand Valley State UniversityMuskegonUSA

Personalised recommendations